Rifleman Breeding System: A Study

The research on New Zealand Riflemen ( Acanthisitta granti ), tiny nesting forest dwellers weighing just 5-8g, builds upon Gray's (1969) work, which highlighted their protracted breeding cycle and territorial behavior. Fitzgerald and Gaze (pers. comm.) further investigated breeding success and nestling growth rates, revealing that females are larger than males—a reversed sexual dimorphism that this study examines. The study's primary location is near the University of Canterbury Edward Percival Field Station in Kaikoura. Initially, the study area encompassed the entire 240ha reserve. Later, it focused on a smaller 80ha area and a 6ha patch. The study area's climate features significant variability, with periods of cold temperatures, wind, rain, sleet, and even occasional snow, particularly during winter and early spring (September-November). This harsh climate significantly affects the breeding cycle and the energetic demands placed on the birds. The impact of this environment on breeding success and energetic costs is a critical component of the research.

The small size of the Rifleman presents significant energetic challenges. Ricklefs (1974) established a link between thermal conductance and body size, showing smaller birds lose heat faster at low temperatures. Kendeigh et al. (1977) further highlighted that decreased size increases energy stress, proposing a lower size limit constrained by the ability to maintain a metabolic rate of 2.2-2.5 kcal/g/day. Calder's (1974) graphs illustrate a dramatic increase in respiration and heart rate frequency with decreasing body weight below 100g. Non-linear relationships between body weight and metabolism reveal maximal metabolic rates at the smallest sizes. However, even small animals need minimum efficiency ratios (work output to energy intake). Gibb's (1954) observations confirmed that smaller passerines spend a disproportionately larger amount of time foraging, directly impacting energy budgets and the availability of time for other crucial activities like breeding and parental care. The study investigates how these physiological limitations impact various aspects of the Rifleman's life history, including breeding behavior and reproductive success.

The researchers used nest boxes, modified from Gray's (1969) design. Modifications included adding a perch and creating an elliptical entrance hole (20-22mm diameter, 36mm width) to prevent access by stoats ( Mustela erminea ), a major predator. While this modification did not entirely eliminate stoat attacks, it hindered their ability to consume nest contents. Another modification was a rubber lid tie-down to secure the nest box from the bottom, thus preventing entry by larger competitors. The study notes that weta, large (up to 50mm long) nocturnal insects, frequently occupied the nest boxes, sometimes in large numbers (up to 12). Their presence disturbed Riflemen, potentially leading to nest desertion. The researchers addressed this issue by removing weta during nest box inspections. This section highlights the practical challenges of studying this species and the adjustments made to minimize interference from predators and competitors in the study design.

The study begins by highlighting the extraordinary size of Rifleman eggs, representing approximately 19% of the female's body weight. This is near the upper limit for egg size relative to body weight among birds. The demands are further amplified because during the first clutch, a female lays eggs totaling about 85% of her body weight in just eight days. Perrins (1969) suggested that passerines typically utilize daily energy intake for egg production rather than relying on stored reserves. This observation raises questions about the female Rifleman's ability to accumulate the necessary weight (85% or the equivalent dry weight of eggs, about 25% of wet weight according to Kendeigh et al. 1956) before laying. The study explores the energetic implications of this reproductive strategy, particularly considering the challenges of meeting these demands when breeding begins in early spring at Kowhai Bush, a time when food supplies may still be limited and the weather exceptionally cold and wet.

The core of this section focuses on courtship feeding in Riflemen. The amount of food fed to females was estimated in milligrams of dry weight, along with data on self-feeding by both sexes. This allowed estimation of the male's contribution to the female's total food intake. The researchers aimed to determine if the rate of courtship feeding correlated with the predicted energy demands of oogenesis. Unlike some other bird species, courtship feeding in Riflemen lacks elaborate ceremony; food is typically given one at a time, quickly accepted by the female, with the male often emitting a soft chittering sound beforehand. While females sometimes chased males for food, this behavior rarely resulted in acquiring additional resources. The study notes 14 instances of copulation during the courtship-feeding period, beginning 12 days before the first oviposition and ending at the start of incubation. Four instances involved mounting immediately after courtship feeding. In two cases, the same male presented his partner with a feather and once with a piece of moss, behaviors that suggest minimal ritualized courtship displays beyond the exchange of food.

The study acknowledges the limitations of using indirect methods for assessing food consumption, which often rely on visual estimations of prey size. The authors explain their approach, drawing parallels with Royama's (1965) method for Great Tits ( Parus major ), which involved estimating insect and spider size (length and diameter) and deriving dry weight equivalents from a regression line of insect volume against dry weight. In determining calorific equivalents, all taxa in the diet were assigned equal importance when calculating average weights for food-size categories. Any errors introduced by this methodology were expected to affect both sexes equally if there were no dietary differences between males and females. This assumption was supported by subsequent findings that types of food delivered to the nest did not differ between parents (referencing section three), suggesting that male and female feeding ecology was similar. This careful consideration of methodology allows a more robust assessment of the significance of courtship feeding in meeting the reproductive energy demands of the female.

The Rifleman's unusual two-day egg-laying interval is discussed in relation to its effect on the female's energy expenditure. The study contrasts this with the potential energetic consequences of a 24-hour laying interval. The authors use Figure 1-9 to illustrate that the two-day interval limits simultaneous yolk formation to two, one of which is in an early stage of development. Daily egg laying, conversely, would require the production of albumen and shell within 24 hours (the shell gland accommodates only one ovum at a time) and the simultaneous development of three yolks (yolk formation takes 3.5 days). The two-day interval minimizes the demands on the female at any given time; this efficient strategy likely evolved as a mechanism to balance energy expenditure with successful reproduction, especially in challenging environmental conditions like those at Kowhai Bush.

The study compares the foraging behavior of Riflemen with that of Brown Creepers and Grey Warblers. Observations indicate that unlike Grey Warblers, neither Riflemen nor Brown Creepers can effectively hover while foraging. While Riflemen attempt to hover, they are unable to remain stationary. This foraging difference, coupled with a potential earlier abundance of exploitable food for Grey Warblers, may give Grey Warblers a competitive advantage, enabling earlier breeding. The fact that Riflemen and Brown Creepers breed around the same time supports the hypothesis that their similar foraging limitations shape their reproductive timing. The crucial difference is the reduced time spent in flight for Riflemen and Brown Creepers compared to Grey Warblers, potentially reducing energy expenditure and influencing their breeding strategies.

Riflemen typically nest in enclosed cavities with small (11-30mm) openings, often in hollows of dead or dying timber. The study also documented four instances of underground nesting, two in old rabbit burrows and two more amongst dead leaves under Cabbage Trees (Cordyline australis). These diverse nest locations highlight the adaptability of the species in finding suitable nesting sites, which may be a critical factor influencing their breeding success and energy expenditure. The type of nesting cavity chosen can have significant effects on insulation, protection from predators, and the overall energy required to maintain a suitable microclimate for egg development.

The first clutches of five eggs weighed approximately the same as an average female and about 120% of an average male's body weight. This large egg mass, relative to the bird's size, necessitates maintaining a precise incubation temperature of roughly 35°C, essential for embryo development in passerines (Kendeigh 1963). The study argues that the Rifleman's incubation behavior is a direct consequence of this energetic challenge: minimizing the energy cost of a small bird keeping large eggs warm. Maintaining a consistent 35°C requires substantial parental effort, and any decrease in ambient air temperature necessitates increased incubation time and reduced foraging time. This trade-off between thermoregulation and foraging is a critical aspect of the energetic budget during the incubation period.

Jones and Ward's (1976) study on Red-billed Quelea (Quelea quelea) showed a drop in intramuscular protein reserves during egg-laying, recovered during incubation. The female Rifleman likely experiences a similar depletion and recovery process. The male's significant contribution to incubation provides the female with approximately two extra hours of foraging time daily, presumably aiding her recovery from the physiological stress of laying relatively large clutches. The greatest number of simultaneous demands on the birds occurred during the transition from the first clutch nestling period into second clutch incubation. This transition highlights a high degree of parental cooperation. The presence of a brood patch in males, which persists throughout the brooding period, further emphasizes the male's crucial role in incubation. This contrasts with Skutch's (1957) findings of a lack of correlation between male incubation behavior and the presence of a brood patch in passerines. The male's brood patch in Riflemen likely functions as an efficient heat shunt, given the large clutch size and the male's important role in incubation.

The study considers night-time incubation behavior in light of energy expenditure. Walsberg and King (1978a) demonstrated that the resting energy expenditure of incubating White-crowned Sparrows (Zonotrichia leucophrys oriantha) is 15% lower than that of non-incubating birds in the same microclimate. This comparison is relevant because, like Riflemen, only one bird typically occupies the nest at night. This supports the hypothesis that the female benefits from roosting inside the nest to recover from egg laying. However, Mertens' (1980) findings on Great Tits show a contrasting result, reporting heat production two to four times the basal metabolic rate in incubating females. Walsberg (1983) later questioned the validity of Mertens' results, suggesting inconsistencies with his own findings based on oxygen consumption and biophysical models. This illustrates the complexity of measuring and interpreting energetic costs during incubation.

The research examines the relationship between ambient temperature and parental attentiveness during daytime incubation. The study found a strong correlation, indicating that incubation behavior is highly sensitive to the environmental factors affecting egg temperature. The only exception was the first half of the first clutch incubation period, when ambient air temperatures were significantly lower. This lack of correlation might be due to the limited temperature range, making behavioral adjustments for adequate embryo development ineffective. The Riflemen's habit of covering eggs with feathers upon leaving the nest likely reduces egg cooling rates, a behavior also observed by Stead (1932) in Stead's Wren (Xenicus variabilis). The males typically add feathers, possibly to maintain nest thermal insulation, while the birds also remove and dry wet feathers. These behavioral adaptations highlight the importance of nest microclimate maintenance and its impact on the energy budget.

Kendeigh (1973) and Drent (1973) emphasize the importance of energetics in shaping nesting behavior, including incubation costs. Drent hypothesized an upper limit of 25% of productive energy for incubation costs. While controversy exists regarding the precise energetic cost of incubation, most relevant studies suggest that it does require a portion of productive energy. This section concludes that the study's observations on incubation time, nest construction, and behavioral adaptations align with the hypothesis that incubation involves a significant energetic cost for Riflemen, particularly given their small size and the relatively large size of their eggs. Further research is needed to fully quantify the relative contributions of passively utilizing environmental heat and active thermoregulation in meeting the requirements for egg incubation.

The study examined nestling growth, focusing on the period between 3 and 12 days of age when weight gain is most significant. Regression analyses of weight against age, using data from 45 male and 51 female nestlings across multiple seasons, revealed significant growth differences between the sexes (F-test, P<0.05). While culmen and tarsus length growth curves showed no sex differences in the age at which adult dimensions were attained, males reached adult weight approximately one day earlier than females. This subtle difference in growth rate suggests a potential for differential parental investment, although consistent differences in weight variability between the sexes were not observed. The study notes that few measurements were made on nestlings under four days old, and sexing was initially done using spirit ink marks on legs or wings before plumage differences became apparent around 10-12 days of age, using Gray's (1969) description of plumage differences as a guide. Individuals were uniquely color-banded at around 18 days old.

Beyond feeding, the study categorized five other forms of parental care: (1) a parent entering and leaving the nest without food; (2) nest inspection visits; (3) brief perch visits; (4) faecal sac removal; and (5) brooding behavior. These categories suggest a more comprehensive parental investment than mere food provision. Brooding ceased after twelve days, aligning with the homeothermic period for passerines (Ricklefs 1978). While interactions between parents were rare, there is a suggestion of a progressive diminution in agonistic behavior. The equal time spent brooding by both parents implies a balanced distribution of this parental care task. The minimal energetic cost associated with brooding, when contrasted with the considerable energy investment in incubation, further strengthens the hypothesis of a relatively equal division of labor between parents after the initial demanding stages of reproduction.

The study investigated the significant role of helpers in raising second broods. While data on helper contributions were limited (only two regular helper nests were intensively studied), male parents and helpers were found to feed nestlings at a significantly higher rate than female parents. The contribution of helpers was notable, even though limited data prevented a detailed analysis of diurnality or comparison with non-helper nests. The proportion of food delivered by helpers (39% and 28% at two nests) was comparable to single Pygmy Nuthatch helpers (Norris 1958), although less than observed in other studies with multiple helpers (Brown 1970, 1972). The study shows that one benefit of helpers to parents is the reduction in energy expended on feeding young (Brown 1978). Casual helpers sometimes behaved towards unpaired females as if courting, potentially reflecting a mate-acquisition strategy. However, this does not always override the contribution of helpers to rearing young of both sexes, as evidenced by feeding of both male and female offspring in the nest and during post-fledging periods.

Post-fledging, helpers continued to assist, although observation was challenging. The study notes an instance where a helper from the first brood also assisted in the second. Most helpers from the first brood provided only occasional assistance to the second. By the third week post-fledging, self-feeding in juveniles became evident, yet adult feeding continued frequently. Groups often split into smaller units of individuals or pairs, with juveniles engaging in chase-begging behavior for food. By day 21, juveniles took most of their food, though competency varied. Begging behavior included gaping and displaying the buccal cavity, as seen in other species. In Riflemen, this behavior is less conspicuous due to the color of the rictal flange. Even though this behavior was widespread, there was no clear evidence of preferential feeding based on sex, though female juveniles appeared more successful at competing for parental attention.

The study mentions instances where eggs were laid within shorter-than-usual 48-hour intervals, implying that the phenomenon of egg dumping (a female laying an egg in another's nest) might occur in Riflemen, especially since nests were sometimes left unattended during egg-laying. The study notes one case where a female laid three eggs in 63 hours instead of the typical 96 hours. This suggests that even if egg dumping happened before the clutch was complete, the pair would not necessarily abandon the nest. A further example discusses a case where a male helper from the first brood, after his parents disappeared, was seen attempting to feed his neighbor's second brood. This behavior highlights the complex social dynamics and flexibility in parental investment strategies, both within and across family groups.

The study assessed annual survival rates of Riflemen from 1981 to 1984 in the main study area (and from 1982 to 1984 in a pilot area). October 15th, representing mid-spring, served as the anniversary date for survival calculations. Annual censuses were conducted, including birds not initially sighted but observed later in the season. Nest boxes were the primary source of data. Unpaired birds were also counted during nest observations. This methodology, while primarily relying on nest box counts, aimed to obtain a comprehensive estimate of survival rates, acknowledging that the period of highest risk (first-year mortality) may not be fully captured. The findings are discussed in relation to the broader context of adult survival rates among small land passerines in temperate regions (Ricklefs 1972), aiming to understand the potential constraints imposed by survival rates on reproductive strategies and lifespan.

The study addresses the reversed sexual dimorphism in Riflemen, where females are larger than males. This contrasts with the typical pattern in many bird species. The authors discuss this reversed dimorphism in the context of parental investment theory. Fisher's (1958) theory predicts equal parental investment in offspring of each sex due to equal reproductive value. However, if rearing one sex is more costly, natural selection may adjust the sex ratio. Differential offspring mortality before independence can also influence the sex ratio. The study investigated whether differential parental investment in Riflemen was related to the higher energetic cost of raising females due to their larger size. Regressions of weight on age (3-12 days) for males and females indicated a significant difference in growth trajectory between the sexes, with males reaching adult weight about a day earlier, with this growth difference investigated in the context of differential maturation and its energetic costs to the parents.

The study explores the relationship between clutch size, environmental resources, and reproductive effort. Schaffer's (1974) model suggests that environmental uncertainty can reduce optimal brood size compared to the optimum under average conditions. This aligns with Merton and Westwood's (1977) assertion that many passerines operate within energy thresholds, limiting clutch size to the number of chicks successfully reared. The study considers whether environmental uncertainty influences Rifleman clutch size and whether this contributes to the observed pattern of sexual dimorphism. The authors propose that if environmental uncertainty reduces brood size, the parents likely have sufficient latitude in reproductive effort to manage the sexual size dimorphism, where females are considerably larger. This suggests the evolutionary pressures favoring larger females despite the greater energetic costs to the parents in such an environment.

The study compares Riflemen survival and life history strategies with other passerines in Kowhai Bush, particularly Grey Warblers. Gill's estimate of Grey Warbler life expectancy is considered an overestimate as it doesn’t account for high first-year mortality. Even with this correction, Riflemen appear to have a shorter life expectancy than Grey Warblers. The estimated mortality rate of Riflemen falls within the 40-60% range for adult survival among small land passerines in temperate regions (Ricklefs 1972). This shorter lifespan suggests a greater time constraint for breeding, potentially leading to different evolutionary pressures compared to Grey Warblers. This difference in lifespan may drive the evolution of larger females in Riflemen to maximize fecundity within a limited number of breeding attempts, making it a key adaptive characteristic within the context of environmental constraints and the high energetic demands associated with reproduction.

The study concludes that the larger body size of female Riflemen, despite the energetic demands of egg production, potentially facilitates increased fecundity. This is balanced by a lower parental investment in males, whose smaller size allows them to cope with the climate and the absence of egg-laying demands. A sex-biased primary sex ratio does not emerge as each sex has equal breeding opportunities and future reproductive value. Differential parental investment is necessary to optimize reproductive value for parents in future generations, maximizing fecundity while maintaining equal average expected reproductive lifespans for both male and female offspring. This reflects an efficient strategy for maximizing reproductive success in a species with limited resources and significant energetic constraints due to its small size, adapted to a challenging environment.

This section frames nest building as a form of parental effort, acknowledging the energy expenditure involved. The study doesn't provide detailed descriptions of nest construction in this section, but it does mention that the males were mainly responsible for adding feathers to the nest, probably to maintain thermal insulation, and that many nests tended to become damp, which would reduce the nest's heat-retentive properties. This observation underscores the importance of nest maintenance and its potential energetic costs, especially in a cold and wet environment like Kowhai Bush. The study implicitly links nest building to the broader energetic demands of the breeding cycle, emphasizing it as a factor that contributes to the overall energy budget of the parent birds. The energy investment in this activity is not quantified but is stated as an energy outlay for the parents.

Territorial behavior is also recognized as a form of parental effort, requiring energy expenditure for defense. The study does not offer detailed information on the specific energetic costs associated with territorial defense in this section but mentions that territorial behaviour is one of two main characteristics of breeding highlighted in Gray's (1969) work. This implies that the energy expended in defending a territory is an additional factor contributing to the overall energetic demands of the breeding season. This activity is discussed in the context of other breeding activities which involve an energy outlay for parents. The energetic cost of territoriality is implicitly linked to the constraints on time and resources faced by these small birds, potentially influencing breeding success and the overall reproductive strategy.

The section considers moult, the process of feather replacement, as an energy-demanding activity affecting individual birds, and how its timing may interact with parental effort. The study suggests that the relative onset of moult between male and female parents could be influenced by the trade-off between parental care and self-maintenance. If the male parent shoulders most of the feeding demands for a second brood, its moult might be delayed relative to the female. This hypothesis highlights a potential conflict between the demands of current reproduction and the individual's need for self-maintenance. The study does not provide specific data on moult timing in this section but raises it as a relevant aspect of the broader energy budget and the balance between parental investment and individual survival during the breeding cycle.