Partial Incubation in Birds: Its Occurrence, Function, and Quantification

Abstract

Early Studies of Incubation behavior acknowledged the existence of a less regular form of incubation that can occur from the beginning of egg laying to shortly after clutch completion. It has been variously termed “partial incubation” (Putnam 1949, Seel 1968, Ashkenazie and Safriel 1979), “brooding” (Barth 1955), “intermittent incubation” (Samuel 1971), “irregular incubation” (Beer 1962), or “nonrhythmic incubation” (Morton et al. 1972). This form of incubation has been described from visual observations of adults sitting on the nest less regularly, and from egg temperatures that are lower and more variable than those typically attained after clutch completion (Barth 1955, Brackbill 1958, Kendeigh 1963, Barrett 1980, Morton and Pereyra 1985). We refer to this little-understood behavior as “partial incubation” because it is characterized by a reduced amount of time during egg laying that parents sit on and warm their eggs, compared with the amount and intensity of incubation they provide later in the nesting cycle after the clutch is complete. Partial incubation is a common way for birds to initiate incubation. The onset of incubation, the moment at which a bird begins to incubate a clutch, is a critical event in the avian nesting cycle because it has important effects on fitness, as noted more than half a century ago by David Lack (1947). Incubation onset can affect hatching success and hatching patterns (Nilsson and Svensson 1993, Wang and Beissinger 2009), nestling growth and development (Slagsvold et al. 1995, Bitton et al. 2006), fledging success (Hébert 1993, Hébert and McNeil 1999), and post-fledging survival and recruitment (Cam et al. 2003). Not only can the onset of incubation affect adult reproductive rates, but it also influences and is influenced by parental body condition and survival (Hanssen et al. 2002). Yet the onset of incubation is rarely described and even less commonly quantified, and methods of determining incubation onset have not been standardized among studies or species. In this review, we (1) clarify terminology for the onset of incubation, refine the concept of partial incubation, and summarize the prevalence of partial incubation. We then (2) examine the potential functions of partial incubation, (3) map individual-level patterns of partial incubation from previous studies onto a recently developed typology of patterns for the onset of incubation (Wang and Beissinger 2009), and examine intraspecific variability and compare interspecific data with respect to taxonomic and ecological diversity. We also (4) provide a standardized method for determining the individual onset of full incubation, using complete records of nest attendance or incubation from the start of laying to beyond clutch completion. Our goal is to show how data from disparate studies can be used to test hypotheses about the function of partial incubation. Finally, we (5) offer questions that may prove to be fertile areas of research and suggest ways to standardize future data collection and analysis to benefit common research goals. The terms “incubation” and “nest attendance” have at times been used interchangeably (Table 1). Beer (1964) defined incubation as “the process by which the heat necessary for embryonic development is transferred to an egg after it has been laid” (cited in Drent 1975). Early nest attendance that resembles incubation may not effectively warm eggs because of gradual brood-patch development (Bailey 1952, Beer 1962, Massaro et al. 2006). Beer (1962) noted that two things are being talked about and are seldom distinguished: the period during which incubation responses are shown by the parents and the period of effective incubation as indicated by the time taken for the development of an embryo. [Emphasis added] A second conceptual duality, related to the intensity of incubation behavior, is that of “partial” versus “full.” Full incubation typically refers to the intensity of nest attendance or incubation achieved around or after clutch completion (whether measured as percentage of daily attentiveness or mean daily egg temperature). Full incubation has been variously named (Table 1) to highlight its differences from partial incubation (i.e., less regular incubation mixed with nest attendance during the laying period). The distinction between full and partial incubation is important, because the factors that affect embryo survival may differ before and after clutch completion. For example, eggs exposed to cold temperatures can survive well for several days if they were recently laid, but not if their embryos are older and well developed (Webb 1987). A few uncommon examples deserve mention here. Full incubation can occur well before laying is complete (such as in species that hatch asynchronously), but species that hatch asynchronously may still display lower levels of incubation during the early laying period (Grenier and Beissinger 1999). Species with a clutch size of one may also display partial incubation, because a plateau in the daily proportion of time spent in incubation (Massaro et al. 2006) or in mean daily egg temperatures (Barrett 1980) may occur much later than the day of egg laying. Terms used to describe partial and full incubation. Terms used to describe partial and full incubation. It may often be useful to consider partial incubation behavior separately for day and night, because diurnal and noctural nest attendance or incubation often differ (Wilson and Verbeek 1995, Clotfelter and Yasukawa 1999, Hepp 2004). Diurnal measurements could start and end with the active day, as determined by the behavior of the adult; they could follow a fixed period or be determined by the length of civil twilight. Nocturnal measurements would then simply be the complement of the times circumscribed by diurnal measurements. Some researchers may prefer to use a 24-h period, as would be appropriate for polar-breeding species. We conducted a literature search using the terms “partial incubation” and “incubation onset” in the Web of Science and in the full text of journals in the Searchable Ornithological Research Archive (SORA). The search resulted in 97 papers with information on the onset of incubation in 103 species—some of which were studied multiple times, to yield a total of 123 incubation onset samples (online Appendix; see Acknowledgments). We used information on onset as presented by the authors' own definitions or calculations, or as judged from data shown in published tables and figures. If partial or full onset was not specified by the author(s), we used the earliest day of any nest attendance or incubation as the onset of partial incubation, and the first day that attentiveness or egg temperature reached approximately the mean level after clutch completion as the onset of full incubation. We also abstracted data on developmental mode, hatching pattern, sample size for the onset of incubation, field and statistical methods, and the egg with which collection of incubation data started (online Appendix). Partial incubation appears to be common during the laying period. Within studies that examined the onset of full incubation in 103 species, 50 species (48.5%) exhibited partial incubation. Among those species that exhibited partial incubation, a disproportionate number (χ2 = 8.35, df = 2, P = 0.015) initiated partial incubation on the day the first egg was laid (27 species, 54.0%), compared with those that started on the day the second egg was laid (13 species, 26.0%) or later (10 species, 20.0%). Thus, partial incubation is common and often begins with the laying of the first egg. Methods of data collection influenced whether partial incubation was detected. The percentage of samples that detected partial incubation was greater when data collection began on the day the first egg was laid compared with later in the laying sequence (27.6% vs. 16.3%, χ2 = 3.6, df = 1, P = 0.057), as well as when data collection was continuous (e.g., egg temperature recordings) rather than discontinuous (e.g., nest checks) (29.3% vs. 14.6%, χ2 = 6.0, df = 1, P = 0.014). Seventy-seven percent of samples using both criteria (n = 20 of 26) detected partial incubation. The body of literature on incubation onset is not a random sample. Passerines dominated the data set (67 of 123 samples, 54%), but studies that used continuous data collection were most commonly of precocial species (12 of 27,44%) (online Appendix). Tropical-zone species were underrepresented compared with temperate-zone species (11.4% vs. 56.1% of 123 samples). However, hatching patterns were generally evenly distributed among synchronous species, asynchronous species, and species that spanned both categories. Many possible adaptive functions of partial incubation could be accomplished with or without the transfer of heat necessary for embryonic development (Table 2). Adaptive functions of partial incubation that would not require embryo development include increasing adult survival or reducing adult energy expenditure, preventing egg loss, and maintaining egg viability. Partial incubation that induces embryonic development could also accomplish any of these functions, because incubation usually requires nest attendance, although warm ambient temperatures can result in embryonic development in the absence of nest attendance. Functions that do not require incubation.—Partial incubation may benefit adult survival or condition simply through nest attendance. The nest site may provide better protection from predators (Wiebe and Martin 1998) or a more favorable microclimate than other locations (Amat and Masero 2004, Pendlebury and Bryant 2005, D'Alba et al. 2009). For example, European tits roost in the nest during the laying period without raising eggs to incubation temperatures (Haftorn 1978, 1979, 1981). Partial incubation for this purpose does not require physical contact with the eggs; indeed, some species stand over the eggs in the nest cup (Brackbill 1958, Beer 1962, Haftorn 1978, Allen 1980, Haftorn and Reinertsen 1982). Nest attendance may also prevent egg loss from predation, nest-site takeover, or brood parasitism. If partial incubation serves these functions, early nest attendance would be predicted in populations with intense competition for nest sites (Beissinger et al. 1998), intraspecific or interspecific brood parasitism (Clotfelter and Yasukawa 1999), or high rates of egg predation in relation to adult mortality (Andersson and Waldeck 2006, Kreisinger and Albrecht 2008, Martin and Briskie 2009). Functions that may require incubation.—Partial incubation could maintain egg viability (Table 2), which can be preserved by either nest attendance or true incubation. Although surprisingly resistant to environmental exposure, avian eggs can perish under immediate threats of constant wetting, temperatures or temperatures and and 1972). Nest attendance can eggs from or (Morton and Pereyra as well as from and heat functions that early nest attendance is during environmental or in to these viability over time under ambient in a of avian et al. Beissinger et al. 2005, Wang et al. because of two and to ambient that growth on as a can the of egg by and et al. nest attendance can the of egg et al. et al. and may the of that a of egg et al. Early nest attendance also onto eggs that may or et al. et al. 2009). Incubation that egg temperatures can an in that has et al. of eggs to temperatures the temperature which development but the for incubation can embryonic development and hatching (Webb In these incubation may be to prevent to the viability can also during to temperatures 1993, Wang et al. because of in and In this partial incubation could the embryo to an early of development that is more resistant to in ambient temperature functions that partial incubation occur when ambient could egg viability during the laying period. However, much of the research on embryonic responses to in temperature has been on species, and more in studies of birds are Functions that require the functions of egg loss, and of egg can also be if partial incubation to embryonic However, or maintaining embryonic development is to adults et al. and Martin et al. developmental and et al. and the of time spent in the incubation, and nestling of the nesting cycle and Beissinger Thus, and may be more to when partial incubation embryonic adaptive functions of partial incubation. adaptive functions of partial incubation. For example, partial incubation in and often embryonic development but does not hatching eggs of precocial species to hatch with the of the clutch when incubation during the laying period (e.g., and and 1999). Partial incubation the incubation period after clutch which the period for (Hanssen et al. at the of eggs that hatch in a and less developed and and 1999). that to during the incubation period may still body and a incubation period would benefit adult body Partial incubation may also maintain the viability of eggs by embryo because eggs viability under ambient et al. Partial incubation that to embryonic development hatching maintaining egg viability and preventing nest-site in the et al. and Beissinger 1999). Thus, egg survival and viability benefit from partial incubation, but the survival of early is over that of later It is important to whether partial incubation embryonic in which the effects of partial incubation can be more The onset of incubation has been in ways (Table or not partial incubation is detected is on the method of data about the function of partial incubation are when incubation can be from nest attendance by the use of two methods that temperature and nest attendance (e.g., Barrett The way to incubation is to the temperature of a egg in the nest and Haftorn 1978, 1979, and and Morton Haftorn and Reinertsen Morton and Pereyra 1985). However, temperatures are not for nest attendance. of the egg can the and or times of incubation and to during high ambient temperatures Wang and nest attendance may be more from nest temperatures 1980, and Verbeek 1995, and et al. and Beissinger 1999, et al. et al. from temperatures of eggs in (Barth 1955, and 1999, and 1999, and Hepp et al. et al. et al. Hepp 2004, and 2004, et al. or of the attendance of adults (Haftorn 1978, Wang and 2009). Incubation can then be from nest attendance by when egg temperatures are (e.g., Barrett Methods used to data on the onset of incubation. Methods used to data on the onset of incubation. observations of parental behavior at can provide continuous records of nest attendance, as well as information as egg egg or and incubation have been at (Putnam 1949, Brackbill 1958, 1962, et al. and at multiple in an et al. However, generally do not provide This is also true of Ashkenazie and Safriel 1979), and (Haftorn 1978, the are with Haftorn and Reinertsen Wang and 2009). research that nest attendance can be less regular than is often (Wang and Beissinger 2009). data collection records the time that adults or from the reducing continuous to records of nest attendance. have used event under the nest et al. and 1993, and et al. and and and to nest attendance for multiple data are the to but they typically sample nest attendance rather than incubation, which requires that a bird in the nest to be in contact with the data collection is less for early incubation but is The most method for determining the onset of incubation is by whether eggs are warm or cold to the during a nest Lack and Lack Seel 1968, 1979, et al. 1993, Clotfelter and Yasukawa 1999, and studies using this method are with the onset of full incubation. This method that eggs are before the start of incubation, and that incubation begins the eggs are at a temperature that is warm to the However, both have been in studies that the nest from the start of egg laying. or visual observations are method of data collection (Beer 1962, and 1980, and Hébert and and on their of the laying period, they can the as the method for the onset of incubation. observations are more to hypotheses to full incubation and Martin rather than the development of incubation behavior over multiple studies on the species how the of data collection influences when partial incubation is detected. early of the partial incubation with the egg clutch size = = using daily nest later studies using temperatures incubation from the (Haftorn to the egg (Haftorn and Reinertsen 1982). In the partial incubation started with the first egg in a that daily nest with visual (Morton et al. as well as when egg temperatures were and Morton Thus, discontinuous data collection may with continuous methods if the is We recently a in developmental of nest attendance to full incubation in (Wang and Beissinger 2009), with high in individual a species as well as in the of among species. individual were “incubation onset using a typology on criteria that describe patterns of partial incubation that can be to species 1). For an individual bird that started with of the day and in with day was as a pattern, a bird that initiated incubation at and achieved the of full incubation a few days was as a In both of these incubation 1). We termed the incubation onset patterns that and (Wang and Beissinger 2009). patterns that not have an in were termed and 1). patterns were on the of their incubation not and 1). We used this typology to patterns from published on from species (n = in to the species (n = used to the typology (Wang and Beissinger (Table We whether patterns of individual onset by of hatching pattern, and taxonomic The are for species in which nest attendance during the laying period is effective incubation. We predicted that precocial species with hatch (e.g., and and would have partial incubation and a the other precocial species without hatch would be to have incubation patterns that start with the egg of a clutch, to that eggs the effective incubation. In with the only patterns (Table and the precocial the exhibited only patterns for the onset of full incubation to whether or not incubation whether the and the and of For the is days or to the completion of laying or on the second day or after full incubation and the is the proportion of the day or The patterns were on not and The data examined for nest started with the day or of incubation shown are The and patterns could have one or more in incubation. from Wang and Beissinger in full diurnal and of in are size is for species for which data were = The measured by is shown as either nest attendance or incubation in full diurnal and of in are size is for species for which data were = The measured by is shown as either nest attendance or incubation The are less when nest attendance be from effective incubation. that hatching species would be more to display patterns that start with the but any of is possible if nest attendance does not embryo of the species could be because the end of hatching from these studies The exhibited only the the other species from previous and patterns more than hatching species are more to have nest attendance that effective incubation. Although any of can be the amount of incubation then be in the of hatching hatching species not show patterns of incubation The exhibited the was by patterns and the by Although nest attendance was with the of hatching in the (Wiebe et al. and with hatching in the (Grenier and Beissinger 1999), it not for hatching in the and Some patterns to be of to the individual or laying period, as body condition or environmental (Wiebe et al. and may result in hatching success (Wang and Beissinger 2009). We these patterns the and 1). that these would not with of hatching pattern, or taxonomic The of patterns was generally less common and in was the common its patterns in only one individual from of species. these patterns to be the result of on adult behavior rather than or in species in which nest attendance during the laying in effective incubation, patterns of the onset of incubation hatching patterns and the of hatching these when nest attendance in the laying does not with effective incubation. If individual is as as these data and taxonomic factors may developmental of incubation at criteria for determining the onset of full incubation would interspecific of incubation from studies using disparate methods of incubation. We using a lower of daily or with the day or after clutch as a for the onset of full incubation (Wang and Beissinger 2009). If egg temperatures are then the lower of the mean daily egg temperature after clutch completion could be This is in relation to the incubation behavior egg at nest after the laying period, and studies have by daily attentiveness or mean egg temperatures through the laying and incubation the of are few on daily attentiveness during and well the laying period. as when the onset of incubation researchers have used either the first egg as the or the egg as the The often on the hatching pattern, because asynchronous species commonly full incubation to the first half of the laying period and synchronous species start full incubation in the second half of the laying period. The onset of partial incubation is often using the first egg as the because onset is more to occur early in the laying period. eggs that have the with to the egg can have of eggs on the clutch We a that both of (Table The can be to of to or more and to both of the We that this for in the The of in incubation onset patterns to be determined (Wang and Beissinger 2009). include that or on a in environmental or on among or body and through environmental or can in observations as well as that are by as et al. 2002). For differences in and can be to fixed as and or random effects on individual as condition et al. 2006). that as ambient and can be as multiple to be (e.g., or with environmental effects over an for the onset of incubation. For species with laying of day, would onset for the day on which the egg is For species with laying greater than day, would the number of eggs in the nest at For of more than eggs, the would be as for eggs laid in an to fixed to egg for clutch some in a terms that may be on the other clutch in a For if greater than egg began full incubation with the egg laid, the clutch may be to have an onset of incubation with the egg laid of the first egg laid, for of for the onset of incubation. For species with laying of day, would onset for the day on which the egg is For species with laying greater than day, would the number of eggs in the nest at For of more than eggs, the would be as for eggs laid in an to fixed to egg for clutch some in a terms that may be on the other clutch in a For if greater than egg began full incubation with the egg laid, the clutch may be to have an onset of incubation with the egg laid of the first egg laid, for of The and of partial incubation are Although partial incubation is more common than is on it is or it influences on partial incubation also questions about patterns of full incubation and environmental factors provide the of in incubation and may also on the of incubation data related to in the onset of incubation could a of questions at both the intraspecific and interspecific intraspecific in the onset of incubation with the size of a or with variability in during the partial incubation species, or are some less in this does partial incubation with the proportion of to predators or between and species, or between species with versus the partial incubation can be as the of during the laying period and Morton et al. 2006). A gradual in often a gradual in incubation individual of incubation during egg laying then those of levels et al. This that incubation with which in may be related to individual as body and in nest attendance or incubation are by in levels has not been studied et al. 2006). In species in which both levels high during from the nest et al. which interspecific variability in the between and parental Species with incubation may have onset patterns that are less to in the development of incubation a the among adult and Not only do daily in the of energy or time to or but these affect survival and (Wang and Beissinger 2009). patterns in the onset of incubation with other reproductive as clutch size and to and environmental a reproductive the for the onset of incubation may provide a the of hatching on the environmental either nest attendance or true incubation may be necessary to egg viability. the and patterns of early incubation may in hatching and and clutch size et al. 2006, et al. 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