Parental care in a sexually monomorphic Picid, the Red-headed Woodpecker
 
Cuidado parental un ave sexualmente monomórfica, el carpintero de cabeza roja

L. Abigail Walter ¹ , Catherine Viverette ² and Lesley Bulluck ²

• Abstract
• Introduction
• Methods
  • Study site
  • Banding methods
  • Monitoring nests
  • Recording parental care behavior observations
  • Parental care analyses
• Results
  • Nest monitoring and chick development
  • Parental care
• Discussion
  • Conclusion
• Responses to this article
• Acknowledgments
• Data availability
• Literature cited

INTRODUCTION

Breeding success in socially monogamous pairs of birds is maximized when parental care is coordinated between males and females (Emlen and Oring 1977). Shared parental care is demonstrated by 81% of bird species, yet the care contributed by each sex is rarely equal (Mock and Fujioka 1990, Cockburn 2006). Division of parental care can be influenced by a species’ mode of nestling development and whether the sexes are monomorphic. Male parental care is more common in species with altricial young, in which the amount of development and growth required between hatching and fledging is greater than precocial young (Ketterson and Nolan 1994). Also, males of sexually monomorphic species tend to provide a greater proportion of parental care compared to males of dimorphic species (Verner and Willson 1969, Pierotti and Annett 1993, Ketterson and Nolan 1994, Badyaev and Hill 2003). In passerines (Passeriformes; an order of birds with altricial young), male nestling provisioning is common in both monomorphic and dimorphic species, and male incubation is more prevalent in North American monomorphic families than dimorphic families (Verner and Willson 1969, Ketterson and Nolan 1994). However, male care during both the incubation and brooding stages is not common in most dimorphic non-passerine families with altricial young, with an exception of the family Picidae (woodpeckers; Wiebe and Elchuk 2003, Rossmanith et al. 2009, Schroeder et al. 2013).

Biparental care has been observed in socially monogamous and dimorphic woodpecker species including Northern Flickers (Colaptes auratus, Wiebe and Elchuk 2003), Golden-fronted Woodpeckers (Melanerpes aurifrons, Schroeder et al. 2013), Ladder-backed Woodpeckers (Dryobates scalaris, Schroeder et al. 2013), White-headed Woodpeckers (Picoides albolarvatus, Kozma and Kroll 2013), Hairy Woodpeckers (Leuconotopicus villosus, Kozma and Kroll 2013), and Lesser Spotted Woodpeckers (Picoides minor, Wiktander et al. 2000, Rossmanith et al. 2009). Male woodpeckers sometimes incubate at equal or greater proportions compared to females and almost always incubate and brood nocturnally (Vehrencamp 2000, Pechacek et al. 2005). Both sexes brood offspring diurnally (Wiktander et al. 2000, Rossmanith et al. 2009, Chazarreta et al. 2011). Males also clean the nest of fecal material (Rossmanith et al. 2009, Chazarreta et al. 2011, Kozma and Kroll 2013, Gow et al. 2015, Tremblay et al. 2016) and help females to provision young (Jackson 1976b, Rossmanith et al. 2009, Chazarreta et al. 2011, Loverin et al. 2021). The high proportion of male parental care in woodpeckers could be a result of limitations imposed by nest substrate and cavity availability (Mock and Fujioka 1990), the demanding needs of altricial young (Temrin and Tullberg 1995), and/or certainty of paternity (Møller and Birkhead 1993, Matysioková and Remeš 2013). Woodpeckers face time and energetic constraints in excavating nest cavities and defending them from competitors and predators (Jackson 1976a, Kilham 1977, Ingold 1989). Additional demands for time come after a clutch is laid; offspring in North American species of woodpeckers require anywhere between 35-48 days of care from egg to fledging (Jackson 1976b). During this time, testosterone in male birds and extra-pair copulations are reduced (Michalek and Winkler 2001, Schwagmeyer et al. 2005) and male woodpeckers may provide parental care due to certainty of paternity (Møller and Birkhead 1993, Matysioková and Remeš 2013). Indeed, studies that have assessed paternity in woodpeckers indicate extra-pair young are rare (Haig et al. 1994, Michalek and Winkler 2001, Pechacek et al. 2005, Li et al. 2009, Kellam 2014).

Despite the general understanding that males in monomorphic bird species and dimorphic woodpeckers tend to provide high levels of parental care, little is known about the allocation of parental care between sexes in monomorphic woodpeckers. Woodpeckers are a family of birds in which males and females are similar in appearance but rarely identical—almost all woodpecker species are sexually dimorphic with regard to size or due to small plumage differences. The Lewis’s Woodpecker (Melanerpes lewis) and Red-headed Woodpecker (Melanerpes erythrocephalus) are the only two species (comprising < 1%) of woodpeckers that are truly monomorphic (Table A1.1). The term “monomorphism” has been used to describe both monochromatic species with slight differences in plumage and monochromatic species with size dimorphism. However, “truly monomorphic” species exhibit no observable differences between males and females; sex cannot be determined using either physiological measurements, plumage characteristics, or even the presence of a brood patch. Sometimes, monomorphic woodpeckers will even exhibit reverse mounting behavior (Kilham 1977, Vierling et al. 2020). Genetic sexing of individual birds using biosamples has made studying and quantifying behaviors in sexually monomorphic species more feasible (Morinha et al. 2012) but has yet to be used to quantify allocation of parental care in either of the truly monomorphic woodpecker species. Quantifying the allocation of parental care in previously under-studied sexually monomorphic species adds valuable insight to our understanding of the evolution of shared parental care and sexual monomorphism in birds. Further, such research expands our understanding of monomorphic species’ natural history and allows for comparison to the significant body of research on parental care behaviors in dimorphic birds.

In this study, we assess whether males and females share parental care equally in a truly monomorphic species, the Red-headed Woodpecker—a socially monogamous bird of conservation concern (Frei et al. 2020, U.S. Fish and Wildlife Service 2021). We hypothesize that males and females will contribute relatively equally to diurnal parental care duties and exhibit similar allocation of effort as seen in dimorphic woodpeckers. Specifically, we predict that male and female Red-headed Woodpeckers will contribute equally to diurnal incubation, brooding, and provisioning. We expect males to be the primary parent to clean the nest of nestling fecal material, consistent with other woodpecker species. In addition to parent sex, we also assess whether nestling characteristics (chick age and brood size) as well as exogenous factors (temperature, date, and habitat type) influence parental care behaviors (brooding and provisioning). We predict there will be no difference in provisioning based on exogenous factors, but provisioning rates will increase as brood size and chick age increase. We also predict brooding durations will be reduced when temperatures are higher and as brood size increases and chick age increases. We acknowledge that other sex-specific parental care contributions occur, but are not assessed in this study, such as egg laying, cavity excavation, nocturnal incubation, and nocturnal brooding. We assume that nocturnal incubation and brooding carried out by male woodpeckers is no more energetically expensive than roosting alone, and therefore would not be expected to influence diurnal activities. To conduct our study, we quantify parental care behaviors of individually marked and genetically sexed Red-headed Woodpeckers using video recordings focused on the outside of nest cavities and model whether variation in these parental care behaviors is explained by parent sex, nestling characteristics, and exogenous factors.

METHODS

Study site

We conducted this study at Fort A.P. Hill (38.0718°N, 77.3274°W), a 31000 ha military installation in Caroline County, Virginia, USA. The army base is a mostly natural landscape composed of a complex mosaic of oak savanna, pine savanna, wetland, and closed-canopy forest. Savannas and forests have been managed for decades through prescribed fire and timber harvesting practices.

Due to limitations of shared use with military personnel, we chose several focal areas (delineated and referred to by the U.S. Army as “training areas”) to study Red-headed Woodpeckers. These sites were chosen based on the locations of known nests found during the 2016 summer field season and because they had a mix of open and closed-canopy forests occupied by breeding Red-headed Woodpeckers (Nickley and Bulluck 2019). Habitats were classified as savanna or closed-canopy based on 2016 National Agriculture Imagery Program (NAIP) aerial imagery. Polygons were drawn around areas that were visually determined to be open or closed forest, with a 70% canopy cover threshold to determine habitat type, and vegetation surveys were used to ground-truth the layers (Nickley and Bulluck 2019). Information on vegetation composition in closed-canopy and savanna habitat types can be found in Nickley and Bulluck (2019).

Banding methods

We captured and banded woodpeckers from February to May in 2016, and April to July in 2017 and 2018, using either canopy mist nets or a pole net. Mist nets were elevated with a rope pulley system on living trees adjacent to nest snags to target individuals as they approached or departed nest cavities (Kilgo and Vukovich 2012). The pole net was placed over a nest cavity entrance at dawn. Captured woodpeckers were color-banded with a unique combination of three colors and one U.S. Fish and Wildlife Service aluminum band (Permit No. 23486; U.S. Geological Survey Bird Banding Laboratory, Laurel, Maryland, USA). We recorded body mass and standard body measurements. We collected three breast feathers for genetic sexing by Animal Genetics (Tallahassee, Florida, USA). The sex of banded woodpeckers was unknown to researchers until all field data were collected to eliminate any potential for bias.

Monitoring nests

We monitored nests from mid-April through early August in 2017 and 2018. From April through May we searched for new nest snags (dead trees with a nest cavity) and re-visited previously active nest snags to ascertain if they were still in use. After identifying active nests in 2017, we checked nests by observing parental behavior at the nest cavity for a maximum of 30 min using binoculars. Nests were deemed to have eggs when adults traded incubation shifts or when adults entered the cavity for at least 3 min (Jackson 1976b, Nickley and Bulluck 2019). Nests were categorized as containing chicks when parents started bringing food items to the nest (Jackson 1976b). Starting in July 2017 and throughout all of the 2018 season, we checked nest contents with a cavity inspection camera (IBWO.org, Little Rock, Arkansas, USA) on an extendable 15 m Crain CMR Series Measuring Rod (SECO Manufacturing, Redding, California, USA). We did not check active nests with cavity entrances beyond the limits (> 15 m) of our extendable pole. The cavity camera allowed us to collect data on the nest stage, number of eggs, brood size, chick age, and nest fate with more certainty than our previous observation methods. Before inserting the cavity inspection camera into a nest cavity, we knocked on the snag to flush potentially incubating woodpeckers. We monitored active nests an average of once every 6 days (SD ± 1.83), depending on access to training areas.

We determined the age of chicks using hatch day when possible. When hatch day was not known, we estimated chick age by 1) using a known fledge date (n = 2 where fledging was observed), assuming the nestling period was 26 days (Frei et al. 2020), or 2) comparing cavity camera images of the chicks with an unknown age to cavity camera images of chicks with a known hatch date. Images taken from nest cavities were used to determine and describe developmental milestones such as eye opening, pinfeather emergence, feather development, and additional behaviors that have not yet been published at length for this species (Figs. A2.1-9).

Recording parental care behavior observations

We placed FS400 Flash Memory camcorders (Canon, Ota City, Tokyo, Japan) on tripods within 10 m of nest snags to record parental care behaviors at the nest. Cameras were focused on the nest cavity entrance and recorded video on fair weather days anywhere between 06:35-15:15 from May to August in 2017 and 2018. Because we were interested in sex-specific parental care behavior, we only included videos in our analysis if 1) at least one adult was color-banded and genetically sexed, 2) banded individuals could be identified by their color band combination, and 3) nests in videos during the nestling stage contained a known number of chicks with known age. We identified and timestamped adult woodpecker behaviors at the nest using BORIS (Behavioral Observation Research Interactive Software, Friard and Gamba 2016). We associated behaviors with a woodpecker’s unique color band combination or by name for each unbanded mate, with the assumption that no additional birds were providing parental care. Cooperative breeding was not observed in our system and has only been reported in two nests in a high-density nesting site reliant on utility poles for cavities in Illinois (Atterberry-Jones and Peer 2010). For analysis, we included the following four parental care behaviors in the ethogram: incubating eggs (in-cavity for > 3 min), brooding (in-cavity for > 1 min and not followed by a cleaning event), feeding chicks (delivering a food item to the nest), and nest cleaning (removal of fecal material or soiled wood chips from the nest). Incubation and brooding had duration times while feeding chicks and nest cleaning were point events.

Parental care analyses

We recorded incubation length for each parent during videos of nests with eggs. For nests with chicks, we recorded brooding length, the number of provisioning visits, and the number of cleaning events for each parent. To test for differences in incubation duration between sexes, we used a paired Student’s t-test. We used a Wilcoxon signed-rank test to compare nest cleaning rates between sexes because the data were not normal.

To analyze brooding durations and provisioning counts, we ran generalized linear mixed models (GLMMs) using R package glmmTMB (Brooks et al. 2017). To determine the best distribution to use for our models, we compared model fit (AIC) for the brooding models using a non-zero-inflated Gaussian error distribution, a zero-inflated distribution, and a truncated binomial hurdle model. A hurdle model accounts for a high frequency of true zero observations in the data by first fitting a binomial response (i.e., the nest is brooded or not) and then models the remaining non-zero values separately (Lambert 1992, Martin et al. 2005). Likewise, for the provisioning models (count data) that contained many zeros, we compared model fit using a zero-inflated negative binomial distribution to a Poisson error distribution. For both brooding and provisioning analyses, video length was used as an offset in the models to account for variable recording time among samples (Foster and Bravington 2013).

To model brooding duration and provisioning rate, we compared models that included parent sex, nestling characteristics (chick age and brood size), and exogenous factors (temperature or date and habitat type). Descriptions of models and their associated variables can be found in Table 1. For nestling characteristics, we first assessed whether a linear or quadratic association with chick age was a better predictor of these parental care behaviors. We considered a quadratic effect of chick age because we expected brooding duration and provisioning to vary in a nonlinear fashion as chicks developed. The nestling characteristics of chick age and brood size were included in all models, except for the null model, because these factors are well known to influence parental care in birds (Wiktander et al. 2000, Rossmanith et al. 2009, Musgrove and Wiebe 2014). All models included random effects of woodpecker ID and brood ID because some woodpeckers had more than one nesting attempt and we sometimes recorded parental care at the same nest on different days during the nestling period. For exogenous factors, we included temperature, date, and habitat type as predictors of parental care behaviors. We used date as a predictor in provisioning models. For brooding duration models, we used maximum daily temperature (T_max) as a predictor instead of date because we expected T_max to be a better estimate of brooding time and these two variables were correlated (P < 0.001, t = 5.0, df = 86). Moreover, we chose to use T_max rather than minimum daily temperature (T_min) because our videos were recorded during the warmer half of the day, and because we found T_max and T_min were significantly positively correlated during both the incubation period (P < 0.001, ρ = 0.7) and nestling period (P < 0.001, ρ = 0.5) using the Spearman rank correlation test. Maximum daily temperatures were obtained from the National Oceanic and Atmospheric Administration (NOAA) Global Historical Climatology Network daily dataset (Menne et al. 2012a, Menne et al. 2012b) from the station in Corbin, Virginia, USA (38.2022°N, -77.3747°W) located 8.4 km from our study site. We used habitat type, classified as closed-canopy or savanna, as the second exogenous factor in both brooding and provisioning models. Habitat was included because vegetation characteristics could cause differences in food availability and/or competitors and influence the time budget of parents and their ability to care for their young. Video start time was included in brooding and provisioning models to account for temporal effects on behavior. We assessed a chick age × parent sex interaction for both provisioning rate and brooding duration because we were interested in whether sexes differed in how they adjusted their allocation of effort as chicks matured. Lastly, we assessed a chick age × date interaction for provisioning because we suspected chicks may be fed more earlier in the season than later in the season (when it may be drier and hotter, leading to lower food availability).

Models were ranked using AIC_c, top models were chosen based on the lowest ΔAIC_c value, and models with ΔAIC_c < 2.0 were considered equally supported. Predictions for brooding time and provisioning rate were generated from the top-performing models and then plotted using stats::predict in R (R Core Team 2021). Brooding durations were adjusted using video length to determine brooding min per hr. Provisioning counts were adjusted using each sample’s video length and brood size to calculate provisioning visits per chick per hr. We tested for overdispersion and correct model specification by running diagnostic tests on the scaled residuals using the DHARMa package in R (Hartig 2019). All analyses were conducted in R 4.0.5 (R Core Team 2021).

RESULTS

Nest monitoring and chick development

We monitored a total of 74 Red-headed Woodpecker nesting attempts (broods) in 48 nest cavities; 14 were in closed-canopy forest and 34 in savanna. Out of 35 individual banded woodpeckers, five were seen in both years. Three of those five had a new mate. We observed that two of the five woodpeckers moved to new nest snags in the second year, both with a new mate. Additionally, only two nest snags were re-used in our footage: one by the same pair, and another by the same male with a new female mate. In 2017, we monitored 39 broods of 24 pairs; in 2018 we monitored 35 broods of 26 pairs. We checked 24 (61.5%) of the 2017 broods and 28 (80.0%) of the 2018 broods with a cavity inspection camera. Broods that were not checked with a cavity inspection camera either fledged before we obtained the camera (in 2017) or were too high for the extendable pole. Out of all nests monitored (N = 74 broods), we had nest contents information for 52 (70.2%). Of 13 failed broods, eight (61.5%) failed during the egg stage and five (38.5%) during the chick stage. The cause of these failures is not known. Although we found fewer nests in closed-canopy forest, on average there were more eggs and chicks in closed-canopy nests than in savanna nests (Table 2). Early and late summer broods showed no difference in clutch size (Table 3). We regularly observed two or more brooding attempts by pairs in a breeding season, which is not uncommon (Ingold 1987, Venables and Collopy 1989).

The first egg of the 2018 breeding season was observed on 15 May and the earliest hatch date was observed on 31 May. The latest observed hatch date was 27 July 2018, though our field season did not extend beyond 8 August and later hatch dates are possible. Clutch size ranged from 3-6 eggs, with an average of 4.0 (SD = 0.9, N = 33). We observed up to five chicks in a nest, but this was shortly after hatching, and brood reduction (number of nestlings decreasing between nest checks) was common (44.4% of broods reduced). Mean brood size was 2.3 chicks (SD = 0.8, N = 36). Based on our ethogram, the oldest chicks that an adult “brooded” (in-cavity > 1 min and not followed by a cleaning event) were a pair of 19-day-old nestlings, by a male, for a duration of 6.3 min. Using our best nest check data (all from 2018, in which we observed the first egg laid and checked nests frequently until chicks were near fledge age), we observed that chicks remained in the nest an average of ~31 days before fledging (SD = 3.0, N = 6). The oldest chick observed in a nest was 36 days old, longer than previously reported nestling periods of 27 days (Bent 1939) and 29 days (Yohannes 2017).

Based on a sample of 14 broods that were checked regularly, we observed pinfeathers starting to emerge at 7 days after hatching for a single-chick nest, but for nests with 2-3 chicks, pinfeathers emerged around day 10 (Fig. A2.4, Fig. A2.5). Eyes began to open as slits by day 11-12 and were fully open by day 16 (Fig. A2.5, Fig. A2.6). Chicks were seen clinging to the cavity walls as early as day 11 (Fig. A2.5). Downy feathers covered the nestlings by day 16, but feather tracts were still visible on chicks’ crowns and scapulars (Fig. A2.6). By day 18, feather tracts were no longer visible (Fig. A2.7). Chicks were seen with their heads out of cavity entrances starting on day 16. Chicks were often seen aggressively begging for food out of the cavity entrance for ~1 wk before fledging.

We recorded two chicks fledging from separate nests on video. In one fledge event, the chick was recorded calling with chattering “rrr rrr” contact calls (Short 1982, Jackson 1976a) and its head out of the nest cavity for 5 min before flying out of the nest. In the second instance, the chick was calling with chattering sounds and high begging “chee-chee” calls (Short 1982) as well as pecking at small fungi surrounding the cavity before fledging. Both fledglings had a downward trajectory. A sibling in each nest emerged with a head out of the cavity entrance once the fledglings had departed. Recordings of both fledge events are available via Cornell Laboratory of Ornithology Macaulay Library (https://search.macaulaylibrary.org/catalog?assetId=ML488612,%20ML488613).

Parental care

To assess diurnal incubation rates, we used 35 total hr of video across 10 broods with eggs in nine different nest cavities (7 broods in 2017, 3 broods in 2018, 1 cavity re-used in 2018). We assessed incubation duration for each parent woodpecker (N = 20) from videos ranging 120-237 min in length (mean = 190 ± 50.5 SD). We retained 135 incubation events (duration > 3 min) and excluded one because the parent was unidentifiable. Females incubated at longer intervals (8.3 min ± 5.9 SD, N = 74) than males (6.9 min ± 3.9 SD, N = 61). Incubation durations were summed for each parent in each video, then converted to a rate (min per hr) by dividing by the video length. The diurnal incubation rate by females was about twice as long as males, on average, although this was not statistically significant (P = 0.07, t = 2.0, df = 10, Fig. 1a).

To assess rates of parental care during the nestling stage, we used 128 total hr of high-quality video across 21 broods in 18 different nest cavities (10 broods in 2017 and 11 in 2018) to quantify brooding rates, provisioning counts, and cleaning counts for each parent woodpecker (N = 35). Videos ranged from 41-243 min in length (N = 88), with a mean duration of 174 min (SD ± 51.8). A total of 1650 parental care observations were recorded and 4 (0.2%) observations were excluded from analysis because the parent was unidentifiable. We analyzed a total of 115 brooding events, 1307 provisioning events, and 224 cleaning events. We also counted 214 events categorized as “visits” in which a parent entered the nest cavity, did not stay inside longer than 1 min, and did not leave with a fecal sac. Chick age and date were not correlated (τ = -0.04, P = 0.6, z = -0.6). Parental care did not differ between years; specifically, brooding rates (P = 0.86, U = 941.5), provisioning rates (P = 0.56, U = 1030), and cleaning rates (P = 0.46, U = 877) were not different, so we pooled data from both years. Males cleaned the nest (mean = 0.72 ± 0.12 SE) at a rate (per chick per hr) significantly higher than females (mean = 0.11 ± 0.04 SE, P < 0.001, z = -4.32, V = 38, Fig. 1b).

In the brooding models, the negative binomial hurdle distribution had a better fit than the zero-inflated Gaussian (ΔAIC = 72.1), Poisson hurdle (ΔAIC = 207.1), or Gaussian (ΔAIC = 382.1) distributions. The best-fitting model for brooding included an interaction between parent sex and chick age (Table 4, Fig. 2). Females brood nestlings significantly more than males when chicks are young (< 10 days), but males continue to brood older chicks for short periods. Females brooded diurnally at longer intervals (7.3 min ± 6.0 SD, N = 62) than males (4.3 min ± 2.9 SD, N = 53) and had a maximum diurnal brooding length (30.2 min) twice as long as males (15.1 min). Nestling characteristics and exogenous factors were not supported as important predictors of brooding.

The mean provisioning rate per parent, across all broods and chick ages, was 4.8 (SD ± 3.8) visits per hr and 2.4 (SD ± 1.7) visits per chick per hr. Assuming chicks were provisioned equally, each chick was fed an average of 4.8 times (SD ± 2.7) per hour with the combined effort of both parents. There were seven videos in which one adult in the pair did not provision (these videos had a similar average length, 177 min ± 43.5 SD). In five of the seven cases, the female did not provision, and five of the seven were in savanna habitat.

In the provisioning models, the zero-inflated negative binomial distribution had a better fit than the negative binomial (ΔAIC = 27.2) and Poisson error distribution (ΔAIC = 103.0). Provisioning models with a quadratic term for chick age (i.e., when chick age was squared) performed better than models with a linear effect of chick age (ΔAIC = 7.5). Our highest-ranking provisioning model included a date by chick age interaction (Table 5, Table 6). This model suggests that Red-headed Woodpeckers provision slightly more in early summer (before July 7) compared to late summer (Fig. 3a) and that the highest rates of provisioning are in the middle of the nestling stage. In addition, brood size was an important factor in predicting provisioning rates (Fig. 3b); larger broods are provisioned more than smaller broods.

Although parent sex was not included in the top provisioning model, we did find variation in the proportion of provisioning by each sex at the brood level (Fig. A3.1). We did a post-hoc analysis to see if we could explain the variation in the proportion of provisioning events done by females and found that none of our measured covariates (habitat, time of day, number of chicks, date, chick age, video length, or distance to nearest breeding pair) were significant predictors.

We found no evidence of overdispersion or model misspecification for brooding or provisioning models based on residual plots and diagnostic tests in the DHARMa package (dispersion test P = 0.432 for best performing brooding model; P = 0.72 for the best performing provisioning model).

DISCUSSION

Through video observations of color-banded Red-headed Woodpeckers at the nest, we found diurnal parental care behaviors are shared relatively equally between the sexes of this truly monomorphic species. Specifically, females diurnally incubate and brood young nestlings more than males; we did not find incubation to be significantly greater, although brooding was. Males almost exclusively clean the nest of fecal material, and provisioning rates are equal between the sexes. These results align with what is known about sexually dimorphic woodpecker species. Such consistency between dimorphic and monomorphic species suggests that biparental care is likely more linked to the life history of woodpeckers than to plumage. Male care is critical for reproductive success in woodpeckers due to their role in excavating nest cavities and nocturnally incubating and brooding.

We observed Red-headed Woodpecker females diurnally brood nestlings significantly more and incubate eggs negligibly more than males. Incubation and brooding are considered to have relatively low energy requirements, which could be why females are able to contribute so much time to these activities after laying eggs (Williams 1996). While females brood and incubate, males may be assisting the nest in other ways, such as by defending their territory and nest cavity from diurnal nest predators, cavity usurpers, and other pairs of Red-headed Woodpeckers (Reller 1972, Kilham 1977, Berl et al. 2013). We did not observe more than the occasional European Starling (Sternus vulgaris) at our study site, but often witnessed Red-headed Woodpecker intraspecific aggression. Red-headed Woodpeckers are highly dependent on nest snag availability, which may be clustered across the landscape, and can result in overlapping territories (Kilham 1977, Kilgo and Vukovich 2014). Kilham (1977) noted that males are the primary defender during such agonistic interactions.

The most important factors we found to be associated with brooding rates for Red-headed Woodpeckers are parent sex and chick age. We did not find the exogenous factors of habitat type nor T_max to influence brooding rates, though these covariates were coarse and biased in relation to the time of day we recorded video, which we discuss in more detail below. We expected higher daily temperatures would reduce required brooding time because Red-headed Woodpecker nests are typically in standing dead trees or in dead limbs of living trees in open areas (Frei et al. 2020), thereby receiving more sunlight that could increase the internal nest temperature. However, T_max may have had a minimal impact on cavity temperatures. Tree diameter is one of the strongest factors affecting the maximum and the stability of internal cavity temperature (Wiebe 2001); larger trees insulate nest cavities from temperature fluctuations better than smaller trees. Red-headed Woodpeckers may prefer the use of large (i.e., greater diameter) dead trees for nest cavities (Nickley and Bulluck 2019) partly for this reason. We found females brood chicks during the day until they are ~10 days old, at which point nestlings start to grow pinfeathers and are better able to thermoregulate (Dawson and Evans 1957). Ten days after hatching, males almost exclusively enter the cavity for "brooding" events. Our ethogram classified any time a parent entered the cavity for > 1 min and did not leave with a fecal sac during the nestling stage to be a brooding event. However, cavity entries during the later nestling stage have also been observed in male Black-backed Woodpeckers (Picoides arcticus, Tremblay et al. 2016) and Northern Flickers (Wiebe and Elchuk 2003), and it is thought that rather than brooding, males are likely stimulating nestling defecation and/or adding fresh wood chips by excavating inside the cavity (Backhouse 2005, Chazarreta et al. 2011, Tremblay et al. 2016). This is also likely for our observed “brooding” events by males later in the nestling period.

Males remove fecal material from the nest more than females in many woodpecker species (Wozniak and Mazgajski 2003, Rossmanith et al. 2009, Chazarreta et al. 2011, Kozma and Kroll 2013, Gow et al. 2015, Tremblay et al. 2016). Our result that Red-headed Woodpecker males were the primary nest cleaners is consistent with research in other woodpecker species as well as one study on Red-headed Woodpeckers that used behavioral-based sexing (Venables and Collopy 1989, N = 2 broods). It is not clear why males would be the primary nest cleaners in woodpeckers, but Wozniak and Mazgajski (2003) suggested the color of soiled material inside the cavity may trigger a response in males to remove fecal material and add wood chips to keep it clean. Hormones such as corticosterone can influence rates of nest cleaning, but whether levels of these hormones differ between the sexes in Red-headed Woodpeckers is unknown (Gow et al. 2015). However, one explanation may be that because males nocturnally brood nestlings (Vehrencamp 2000, Pechacek et al. 2005, Chazarreta et al. 2011), they are simply attempting to reduce their own exposure to infection, parasites, and/or predation (Ibáñez-Álamo et al. 2014, Azcárate‐García et al. 2019). In addition, males may allocate more effort to clean the nest to compensate for females’ effort toward egg laying, diurnal incubation, and diurnal brooding of young nestlings. We found males cleaned the nest once every 1.4 hr on average, but females only once every 9.1 hr. Because males were 6.5 times more likely than females to clean the nest of fecal material and soiled wood chips, future studies on marked populations of Red-headed Woodpeckers may be able to use nest cleaning rates as a reliable way to infer parent sex without genetically sexing individuals.

As we predicted, Red-headed Woodpecker provisioning rate varies with the developmental stage of nestlings, peaking around 15 days post-hatching. Provisioning remained relatively high from day 15 until fledging for observations we recorded in the early season, but later in the nestling season, provisioning declined after day 15 post-hatching. Loverin (2021) also found a peak in provisioning of Black-backed Woodpeckers at day 16 of the nestling period and in earlier nests compared with later nests. The decline we observed in provisioning after day 15 in the late season, but not the early season, can be explained by two alternative hypotheses. One is that the availability of food declines as the nesting season progresses, and the other is that larger food items are available later in the season, allowing for fewer provisioning trips to provide the same level of nutrition. We were not able to identify food items nor animal taxon for a large enough portion of parental provisioning trips to include food type or size in our analyses. We are therefore unable to test these two alternative hypotheses to explain the decline in provisioning in later season nests.

Though we did not explicitly include prey type or size in our analyses, we can speak generally about the types of food items brought to nestlings by Red-headed Woodpecker parents in our study system and compared with another recent study. We observed Red-headed Woodpeckers foraging for and provisioning nestlings with insects and arachnids from a variety of taxonomic orders as well as blackberries (Rubus spp.), blueberries (Vaccinium pallidum), and huckleberries (Gaylussacia frondosa, G. baccata). Vukovich and Kilgo (2019) have described Red-headed Woodpecker nestling diet in detail and reported a decrease in the proportion of plant matter fed to nestlings in South Carolina at the end of the breeding season. However, the fruiting species we saw being fed to nestlings at Fort A.P. Hill flower early and produce fruit throughout the summer, suggesting no issue with abundance (Stiles 1980, Pavlovic et al. 2011, Gallinat et al. 2018). Red-headed Woodpeckers are excellent flycatchers that depend on aerial insects to supplement their summer diet of ground-dwelling and arboreal insects and fruit (Conner 1979); it is possible that aerial insect declines across North America (Sánchez-Bayo and Wyckhuys 2019) could be a limiting factor to late-season provisioning. Further study is needed to quantify soft mast production and insect abundance near Red-headed Woodpecker nests to determine if our observed reduction in late-season provisioning rates is common and if so, whether it is a function of food availability or differences in prey type or size.

Although the mean provisioning rate was not different between Red-headed Woodpecker males and females across all observed nests, the ratio of male-to-female provisioning varied quite a bit among broods. In some broods the male was the primary provider while the female was the primary provider in others. This may simply be due to our videos capturing a snapshot in time (a few hours in a day); in other words, this observed variation may be due to chance. In an effort to elucidate if individual variation among broods was random, we conducted a post-hoc analysis. We assessed whether the variation in the proportion of female parental care could be explained by any of our measured covariates but did not find any to show a significant relationship, suggesting this among-brood variation could be due to chance and a product of our short video observations.

There are several limitations to our study that are worthy of mention and provide context for our results. Our primary goal was to quantify how parental care was shared between the sexes in this monomorphic woodpecker. Therefore, our other explanatory variables are quite coarse and do not provide conclusive evidence on the impact of habitat and/or temperature on parental care. We encourage future studies of Red-headed Woodpecker provisioning, and parental care in general, to include more detailed measures of habitat and food availability. Further, our nest observation videos were recorded from the morning to early afternoon on non-rainy days, so we did not capture much variation in our time of day, temperature, or precipitation covariates. Future studies interested in how weather and time of day impact parental care should record observations with a wider variety of weather conditions and times.

Conclusion

Our study is the first to confirm equal biparental care in a truly monomorphic woodpecker species. The proportion of effort male and female Red-headed Woodpeckers dedicate to parental care is not unlike the contributions of many other dimorphic woodpecker species; males almost exclusively clean the nest of fecal material (Wozniak and Mazgajski 2003, Rossmanith et al. 2009, Chazarreta et al. 2011, Kozma and Kroll 2013, Gow et al. 2015, Tremblay et al. 2016). Dimorphic male woodpeckers also help females to provision nestlings (Jackson 1976b, Rossmanith et al. 2009, Chazarreta et al. 2011, Loverin et al. 2021), assist in diurnal incubation (Vehrencamp 2000, Pechacek et al. 2005), and assist in diurnal brooding (Wiktander et al. 2000, Rossmanith et al. 2009, Chazarreta et al. 2011). Red-headed Woodpeckers divide parental care so that males excavate new nest cavities or defend their old ones, provision nestlings, clean the nest of nestling feces, and nocturnally incubate eggs and brood nestlings. Red-headed Woodpecker females produce eggs, provision nestlings, and carry out the majority of diurnal incubation and nestling brooding. This division of labor in Red-headed Woodpeckers likely results in a somewhat equal overall contribution of energy by both sexes, and theory suggests that such equal allocation of effort is most common in species with low levels of parental conflict (i.e., searching for extra-pair mating opportunities, Olson et al. 2007). This study, and others like it, can be used to further understand the link between parental care, parental conflict, and plumage similarities among mates (Verner and Willson 1969), particularly because sexual monomorphism and dimorphism are labile evolutionary traits (Price and Birch 1996).

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