The discovery of hatching and transition to feeding young by male Mountain Bluebirds
Abstract
enIn many bird species, only females incubate the eggs, but both sexes feed nestlings. The means by which males of such species discover hatching and transition to feeding their offspring remains almost completely unexplored. Of particular interest are species with nests whose contents are concealed from view. During June and early July 2015 in the Bighorn Mountains of Wyoming, we used continuous video-recording of nests of cavity-nesting Mountain Bluebirds (Sialia currucoides) to document the transition to feeding young by males. We saw no evidence that females used distinct vocal or visual displays to signal hatching to males. Observing mates carrying eggshells away from, or food into, nest boxes did not appear to trigger provisioning by males. Rather, at all 24 nests observed, males did not begin feeding until they had come to nest boxes and presumably sensed the presence of hatchings directly. Individual males varied, however, in both the manner in which they inspected nest contents and the number of times they did so before starting to feed young. Although most males fully entered nest boxes where they could see, touch, hear, and possibly smell hatchlings (or eggshell parts), other males may have detected hatchlings only by sound or possibly smell while perched at a nest-box entrance. Based on past studies of mice and doves, we suggest that, for provisioning behavior to begin, some kind of direct sensation of offspring may be necessary to activate relevant neurons in the medial preoptic area of the hypothalamus of males, an area of the brain important in parental care. Additional research is necessary to test this, and to examine the effects of factors such as hormone levels and breeding experience on the means and rapidity by which males discover hatching and transition to nestling provisioning.
El descubrimiento del eclosionamiento y la transición para alimentar los pichones en machos de Sialia currucoides
esEn muchas especies de aves tan solo la hembra incuba, pero ambos sexos alimentan a los pichones. La forma en que los machos descubren el eclosionamiento y la transición para alimentar a los neonatos se ha mantenido casi totalmente inexplorado. Son de particular interés especies cuyo contenido del nido queda oculto a la vista. En estudio que se llevó a cabo en las montañas Bighorn, Wyoming, durante junio y julio del 2015, utilizamos video contínuo para documentar la transición de alimentar a los pichones en Sialia currucoides, el cual anida en cavidades. No evidenciamos que las hembras utilizaran distinta vocalización o patrones particulares de conducta para indicar el eclosionamiento. El observar a la pareja cargar los cascarones de los huevos o llevar comida al nido, tampoco pareció estimular la alimentación por parte de machos. En los 24 nidos observados, los machos no comenzaron a alimentar a los pichones hasta que se allegaron a la caja de anidamiento y sintieron, presumiblemente, la presencia de los pichones. Hubo diferencias individuales, en las maneras en que inspeccionaron el nido y el número de visitas, previo a comenzar a alimentar a los pequeños. Aunque la mayoría de los machos entraron en la caja y pudieron observar, tocar, oír y posiblemente oler a los polluelos (o los remanentes de cascarones), otros machos parecen haber detectado los pichones por sonido u olor ya que solo se posaron a la entrada del nido. Basados en estudios previos en ratoncitos y palomas, sugerimos, que para que la conducta de alimentación comience, pudiera ser necesario algún tipo de detección directa de los polluelos para activar las neuronas pertinentes en el área media preóptica del hipotálamo de los machos. Dicha área del cerebro es importante para el cuidado parental. Se necesitan trabajos adicionales, para probar lo indicado y examinar el efecto de factores, como los niveles de testosterona y la experiencia previa reproductiva, en la forma y rapidez en que los machos descubren los neonatos y comienzan a alimentar los mismos.
Although males in many bird species do not incubate eggs, they do feed nestlings, often delivering most of the food to nests when hatchlings are heterothermic and females need to brood extensively. In such species, how do males, given that they do not incubate, discover that hatching has begun? The situation is most intriguing in species where nests and their contents are concealed within some type of cavity. Three hypotheses have been proposed as to how males in these species discover hatching (Skutch 1953a, Johnson et al. 2008). First, females could signal hatching to males. This hypothesis predicts that females produce some unique visual and/or vocal signal shortly after hatching begins that quickly triggers nestling provisioning by males (see Nice and Nice 1932 and Hyde 1939 for possible examples). Second, males may take cues from female behavior, such as carrying eggshell parts away from, or food into, nest cavities. This hypothesis predicts that males routinely begin food delivery after having only observed such behavior by their mate (i.e., before encountering hatchlings themselves). Third, males may have to sense the presence of hatchlings directly before they start repeatedly delivering food to nestlings. Males may, for example, hear vocalizations of the newly hatched young when at or near nest-cavity entrances. Males may also partially or fully enter cavities where they may not only hear but can also see, smell, and/or touch hatchlings (and/or empty eggshells). Males may enter cavities during late incubation for a variety of reasons, including to feed females or check on or guard nest contents. Alternatively, they may have some kind of internal clock that stimulates them to check nest contents or even bring food to nests late in incubation (Nolan 1958). Regardless of how males come to encounter hatchlings, this last hypothesis predicts that males only begin feeding after at least one such encounter occurs.
To date, how males discover hatching has been the subject of a focused study of only one species. In cavity-nesting House Wrens (Troglodytes aedon), Johnson et al. (2008) found no evidence of a “hatching signal” from females to males, and no evidence that males routinely discern hatching by seeing their mates with eggshells or food. Rather, almost all males observed did not begin delivering food to nests until after they had entered nests one or more times and presumably encountered hatchlings themselves. More studies are clearly needed to determine the ways by which male birds discover hatching and transition to feeding. We used continuous video-recording of nests of cavity-nesting Mountain Bluebirds (Sialia currucoides) to further explore this critical juncture in the avian reproductive cycle.
Methods
Study species
Mountain Bluebirds are sexually dimorphic, socially monogamous, insectivorous passerines that breed at elevations up to ~3800 m in western North America (Power and Lombardo 1996). They typically nest in pre-existing tree cavities, but readily use nest boxes. Pairs construct nests of grass with deep cups. Females usually lay clutches of 4–6 eggs, which they alone incubate. Most males feed their incubating mate, but do so sporadically. Eggs typically hatch 13–15 d after the last egg is laid. Hatchlings make intermittent, distinct “peeping” sounds, presumably as part of begging. Only females brood the initially heterothermic hatchlings, but both parents deliver prey to young throughout the nestling and fledgling stages. Parents almost always deliver a single prey item per trip to the nest (Balenger et al. 2007).
Study dates, location, and field methods
We conducted this study during June and early July 2015 on a plateau in the central Bighorn Mountains in Sheridan County, Wyoming (44°46′N, 107°32′W, 2500 m asl). Adult bluebirds were unmarked so ages were not known. All breeding pairs observed used nest boxes mounted on either fence lines or utility poles.
We checked nest contents every other day to track breeding progress. Midway through incubation, we attached a perch made from a ~1-cm-thick piece of wood dowel to the front of nest boxes. Perches were 10–12 cm long and positioned parallel to and ~6 cm away from the front of boxes, such that they were ~4–6 cm below the bottom of box entrances (Fig. S1). This perch simulated a thin, bare tree branch crossing in front of the entrance to a natural nest site. The purpose of the perch was to get adults to stop briefly in view of the video-camera before entering the nest box so we could see if they were carrying food. When parent bluebirds come to feed nestlings, they typically stop on some perch (e.g., branch or fencepost) within 1–2 m of the nest cavity and then (females especially) fly directly to and seemingly through the nest-box entrance in one rapid motion. Our perch successfully encouraged adults to make their last stop at the box entrance. It also allowed males to perch close to, but not at nest-box entrances, but did not seem to alter adult behavior in any other way.
We started video-recording activity at nests 12 d after the laying of the last egg using camcorders (Hi8 8-mm, Sony, Tokyo, Japan). We filmed from the side of nest boxes so we could see items in birds' bills as they stopped on the perch. Cameras were positioned ~1.5–2 m from nest boxes (Fig. S2). Tripods were put in place on the afternoon the day before we began video-taping to habituate birds to a foreign object next to nests. Birds seemed tolerant of cameras even upon first exposure; females typically entered nest boxes to incubate within minutes of our departure.
We began video-taping 20–30 min prior to sunrise. We changed tapes and camera batteries every 4 h, three times during the day, and taped until after dusk. We checked nests for hatching before starting video-cameras at dawn and after each battery change. Upon first encountering hatchlings, we continued video-taping for 4–8 h to ensure that we captured all events leading up to repeated delivery of food by males.
When we arrived in the relative darkness of early dawn, males were usually not in view and females were still in nest boxes. We gently nudged females aside with our fingers to view nest contents. This did not cause females to flush from the box and our activity at this time (or during battery changes later in the day) never seemed to stimulate males to come to nests. In some cases, we found that, by dawn, 1–2 eggs had hatched or were in the process of hatching on the day we began video-taping. In these situations, video evidence suggested that the male was not yet aware of hatching, i.e., he did not appear for >30 min and did not carry food when first arriving at the nest. We included these nests in our analyses. In a few nests, however, we found most or all eggs hatched at dawn on the first day of filming. At these nests, males invariably appeared with food soon after our departure, suggesting hatchlings probably appeared and were discovered by males late on the day before. We excluded these nests from the study. Ultimately, we successfully captured events leading to male provisioning at 24 nests, including 13 nests where all eggs were unhatched when video-taping began and 11 nests where eggs had started hatching shortly before video-taping began.
Data extracted from video-recordings and analysis
We documented the time of each female's entry into, and exit from, nest boxes. We noted whether they carried food into, or eggshells from, the boxes, which indicated that hatching had begun. We also noted the time of each visit to nest boxes by males and their behavior. When males arrived with no food, we noted when they engaged in one or more of the following “investigative” behaviors (Video S1): (1) raising up on extended legs while on the perch and turning an eye and ear towards the nest-box entrance as though trying to look into the box (although they could not have seen nest-cup contents) and/or listen for sounds coming from the box, (2) moving to the nest-box entrance and pulling themselves up such that they could stick their head in the entrance, (3) entering part-way into the nest box, well past the wrist joints, or (4) fully entering the nest box. When males arrived with food, we noted the size of the prey item as small (less than a third the length of the male's beak), medium (no longer than his beak) or large (longer than his beak), and also noted whether they passed food to females through the nest-box entrance, took the food into the nest box, or left with the food.
To test the hypotheses outlined above for how males discover hatching, we first watched for any unique vocal or other type of display behavior on the female's part occurring immediately after hatching and whether any such behavior was followed by male food delivery. If this did not occur, we noted whether males only began food delivery after they had come to nest boxes and had the opportunity to sense the presence of hatchlings directly, or whether males began food delivery after presumably having only observed the female carrying eggshells from, and/or food into, nest boxes.
Results
Cues to hatching from females
No female Mountain Bluebird performed any kind of unique or unusual vocal or visual display from nest box entrances or box perches when hatching occurred. Females did, however, potentially provide males with other cues to hatching at 21 of the 24 nests we observed. At these nests, females made one or more trips from nest boxes with eggshells or into boxes with food before males first came to nest boxes after hatching began. At eight nests, we were either certain that the male saw his mate with eggshells or food at least once (Videos S2 and S3) or video evidence indicated the male was near the nest box when one or more of these events occurred (Videos S4 and S5). In addition, in some cases where females took food into a nest box, males arrived on the box perch immediately thereafter and saw the underside of the female's tail feathers in the nest-box entrance for an extended period of time, indicating that her head was down in the nest cup. At the 13 other nests, females made between one and 10 trips either out of nest boxes with eggshells or into the nest boxes with food after hatching before males first came to the nest boxes, but we were unaware of the location of the males at the time of these events. However, given that males are often near nests and that there were limited number of perches near each nest (e.g., a single set of fence posts or power lines), it seemed likely that males at some of these nests saw their mate with eggshells or food at least once, especially in the seven cases where females made 5–10 such trips before males first came to nests.
Although a substantial fraction of the males that we observed probably saw their mates with eggshells or food, there was no clear evidence at any nest that this alone stimulated males to begin food delivery to hatchlings. In only two of 21 cases where females potentially provided males with cues that hatching had begun did males carry food on their first trip to the nest box. In both cases, however, males appeared to be bringing food for their mates, not the young. Both males carried a prey item that, although typical of the size given to an incubating mate, was much larger than the small prey usually brought to hatchlings. One male passed the prey item to his mate through the nest-box entrance, stuck his head in the box, and then returned ~20 min later without food when his mate was away and stuck his head in the nest-box entrance multiple times. He returned ~2 min later carrying a small prey item and then returned with prey of that size repeatedly thereafter (Video S6). The other male came to the nest-box perch with a large prey item. His mate was absent, however, and, after a pause, the male entered the box. He emerged ~3 min later without the food, and returned ~2 min later with a small prey item and delivered small prey continuously thereafter.
Direct evidence of hatching
At all 24 nests, including the two just described, males began repeated delivery of small prey to nests only after they had had one or more opportunities to sense the presence of hatchlings directly. Males came to nests from 1 to 9 times (median = 2 times) prior to making their first trip to the nest with food seemingly intended for hatchlings. During these trips, males engaged in a total of 1–14 investigative behaviors (median = 4.5). One male started feeding after a single bout of “looking and listening” from the box perch. Eight males started feeding after only sticking their heads in nest-box entrances one or more times (range = 1–9 times, median = 2.5) and one male fed after half-entering the nest box a single time. The remaining 14 males did not feed until after they fully entered the nest box 1–4 times (median = 2 times). The total time that elapsed between the first investigative behavior and the first delivery of prey to hatchlings ranged from 2.3 to 101 min (median = 11 min).
We considered males as having fully transitioned to feeding hatchlings when they made three consecutive trips to the nest with small or medium-sized prey items because, after this, males rarely, if ever, returned to nests without food in the time we observed them. At six of the 24 nests, males delivered small or medium-sized prey only once or twice and then returned to nests without food seemingly to reinvestigate nest contents. Five of these males made 1–4 such additional investigations (sometimes delivering food once or twice in between) before starting to feed regularly. The remaining male, the male that took 101 min to make his first delivery, made 13 such visits, including four trips fully into the nest box. His eggs hatched late in the day and he was still investigating nest contents between occasional deliveries of food when video-taping ended in near darkness, 122 min after his first delivery of food to nestlings. For the remaining 23 males, median time that elapsed between their first investigation and the start of persistent delivery of food to hatchlings was 22 min (mean = 28 min).
Stimulus to visit and inspect nests
Males may have been stimulated to come to nests after hatching by changes in their mate's behavior, e.g., the carrying of eggshells or food. However, we also obtained evidence suggesting that most males visit and check nests with some regularity during incubation, and some males may have discovered hatching during one of these “routine” inspections. At 15 nests, we began video-taping the day before hatching began. We documented male behavior on this day during the first several hours of daylight (mean observation time = 3.5 h, range = 2.6–3.9 h). In addition to trips to the nest to feed their incubating mate, 14 of the 15 males came to nests multiple times without food, averaging 1.4 such visits/h (SD = 0.7, range = 0.5–2.4). During these visits, one male only sat on the box perch, but the 13 other males stuck their heads into nest-box entrances one or more times and five males also partially or fully entered nest boxes.
Discussion
We saw no evidence that female Mountain Bluebirds informed males of hatching through distinct visual or vocal displays at nest sites. This does not preclude the presence of such displays away from nests, but no such display has been reported anecdotally in either Mountain Bluebirds or two congeners, Western (S. mexicana) and Eastern (S. sialis) bluebirds. We also found no clear evidence that observing mates carrying eggshells or food stimulated males to start delivering food to hatchlings. Rather, at all nests observed, males did not appear to start delivering food to hatchlings until after they had come to nest boxes, giving them the opportunity to sense the presence of hatchlings directly. At most nests (14 of 24), males fully entered nest boxes one or more times, allowing them to sense hatchlings (and/or half-shells, if present) through sight, sound, touch, and, possibly, smell (assuming hatchlings and/or shells emit a distinct and detectable odor). At one nest, the male went half-way into the nest entrance where he could do all but touch hatchlings or eggshells. At eight of the remaining nine nests, males only stuck their heads into the nest-box entrances one or more times, and would have been able to hear hatchlings and possibly smell them (or eggshells if present) and possibly see nest-cup contents. Finally, one male started feeding after only perching with his head ~4 cm from the nest-box entrance after, presumably, having only heard hatchlings. Most other males also engaged in bouts of looking/listening from nest-box perches, but always then also stuck their heads into the entrance or entered nest boxes.
Our results are qualitatively consistent with results of previous studies. Skutch (1953a,b) documented events before, during, and after hatching at one or two nests of eight mostly open-nesting passerine species in Costa Rica. He reported that the sight of females carrying or eating eggshells or bringing food to hatchlings seemingly failed to stimulate male provisioning behavior in seven of the eight species. Rather, males typically began food delivery only after seeing hatchlings. As noted above, in the only other study of this type with cavity-nesting House Wrens, 23 of 26 males did not begin food delivery until after they had entered nest cavities, even though most males almost certainly had seen their mates with eggshells, food, or both (Johnson et al. 2008). Also, as with male Mountain Bluebirds in our study, only some male House Wrens began feeding repeatedly after just one nest inspection. The rest made 3–5 inspections and some males, after delivering food once, returned to nests without food to reinspect nest contents before they started to consistently deliver food.
Differences in the time it takes males to start feeding after nest inspection, and in the number of inspections required to trigger persistent feeding by male House Wrens and male Mountain Bluebirds, likely results in part from differences in the number, type, and intensity of cues to hatching available when males made their initial visits to nests. In our study, the number of hatchlings and their behavior (e.g., moving or gaping or vocalizing) as well as the number of half eggshells present, if any, would have differed from nest to nest at the time of initial inspections. The degree to which hatchlings (and/or shells) were still drying would have affected the amount of any tell-tale odor emanating from the nest cup. Finally, in a few cases in our study, females were in nests at the time of a male's initial investigation, which may have made detection of hatchlings less likely.
Differences in male behavior may also have resulted from differences in breeding experience, with more experienced breeders more readily picking up on cues that hatching has begun. Unfortunately, we could not test for effects of experience as we did not know the breeding history of the males we observed. Finally, differences in behavior among males may, at least in part, have resulted from differences in circulating levels of certain hormones, including testosterone and perhaps prolactin (Lynn 2016). In birds, higher levels of testosterone appear to motivate males to engage more in behaviors such as territorial defense and courtship than in parenting (Lynn 2008, Vleck and Vleck 2011).
Our results and those of previous studies suggest that male passerines may, in most cases, need to sense the presence of hatchlings directly before they start delivering food. As discussed by Johnson et al. (2008), this may be necessary to “activate” relevant neurons in the medial preoptic area of the hypothalamus, the seat of parental behavior in birds and mammals (Buntin 1996, Lonstein et al. 2015). Extensive studies on mammals, especially rodents, have shown that, in females, direct exposure to pups induces the expression of certain genes, including fos genes, in neurons in this region of the brain. fos genes code for transcription factors that induce expression of other genes that affect changes in neuron function and, ultimately, behavior (Kuroda et al. 2011). Female mice with experimentally inactivated fos genes fail to show normal parental activities after giving birth (Brown et al. 1996).
Similar studies on birds are unfortunately few. However, Buntin et al. (2006) showed that, in domesticated Ring Doves (Streptopelia risoria), fos expression was higher in brains of male and female parents re-exposed to their own chicks after an absence of 16–18 h than in the brains of parents that remained separated from their chicks (see also Ruscio and Adkins-Regan 2004). These authors also showed that fos expression remained low in individuals deprived of visual (but not auditory or olfactory) contact with their chicks while these chicks were being fed by their mate in an adjacent, but inaccessible, area of the home cage. Buntin et al. (2006: 660) concluded that “visual cues from young are particularly important for neuronal activation in parents.” Based on our findings with Mountain Bluebirds, we speculate that, in other species, especially cavity-nesting species where only females incubate, other kinds of cues from hatchlings, including vocalizations and perhaps odors may also induce the gene expression required for the onset of normal parental behavior in males. We also suggest that differences in male behavior in our study may have resulted in part from inherent differences in the amount and type(s) of sensation required to trigger sufficient neural activity, i.e., gene expression, to result in repeated delivery of food to the nest.
In sum, ours is now the third study to suggest that male songbirds typically must sense hatchlings directly before they transition to making food delivery to hatchlings their priority. More studies of this type will obviously be necessary to determine if this is the norm in passerines and perhaps other types of birds. Studies of how breeding experience and hormone levels affect the transition to feeding young are also needed. Finally, more studies of birds examining the effects of auditory, visual, olfactory, and tactile cues on gene expression and neuronal activation in parental areas of the brain are warranted. Studies of captive species that have nests without easily viewed nest cups would be ideal.
Acknowledgments
Financial support was provided by grants from Towson University's Fisher College of Science and Mathematics, Undergraduate Research Committee, and Faculty Development and Research Committee. Roberta Young of Bear Lodge Resort graciously provided affordable living accommodations at the Bighorn Mountain study site. D. Kozlovsky, R. Hebert, K. Long, A. Krakauer G. Ritchison, M. Reudink, and an anonymous reviewer suggested improvements to the manuscript. To all we are grateful.
