Mass fluctuation in breeding females, males, and helpers of the Florida scrub-jay Aphelocoma coerulescens

Within-day increase in body mass

We observed an increase in body mass daily from morning to afternoon in 27 individuals that were weighed twice in the same day (Fig. 1). The average increase was 0.205 ± 0.117 g/h, with no significant differences between the three social classes (F_2,24 = 2.035, p = 0.15). The mass increase during the examined central hours of the day was best explained by a linear increase (t = 1.691, P < 0.05), while the addition of a quadratic term was not significant (t = 0.354, P = 0.35).

Mean body mass by fortnight and stage of the breeding cycle

The mean mass of jays was influenced by date and stage during the breeding season (Table 1). The mass of females was higher during the first fortnight and the first phase of the breeding stages, then mass values were significantly lower (mixed model ANOVA, five fortnights: F_4,177 = 52.4, p < 0.001; three stages: F_2,162 = 73.1, p < 0.001; Table 1). The mass of females was lower during the nestling stage (t = 5.74, p < 0.001, post hoc comparison with Tukey correction) and the fledgling stage (t = 7.69, p < 0.001) than during incubation. The mass of males and helpers showed significant differences in relation to date (five fortnights, males: F_4,511 = 15.9, p < 0.003; helpers: F_4,244 = 36.1, p < 0.001) and to breeding stage (three stages, males: F_2,439 = 38.2, p < 0.001; helpers: F_2,206 = 38.6, p < 0.001). However, mass in males showed no trend to decrease with time; their mass was highest during the middle fortnight (t = 3.38, p < 0.006) and middle stage (nestlings: t = 2.89, p < 0.004). The mass of helpers was highest in the third and fifth fortnights (t = 5.02 and t = 3.19, p < 0.01) and in the last two stages (nestlings, t = 5.77, p < 0.001; fledglings, t = 5.15, p < 0.001).

Day-to-day fluctuations in mass

Most day-to-day fluctuations in mass were small, most (80%) within 2 g, which is less than 3% of the mass of an adult bird (77 g). The median fluctuation was 0.2 g with a range from −4.0 to +6.4 g. The amplitude of mass fluctuations (Fig. 2) did not vary by date (Mixed-effect model with serial correlation; Julian date: t = 0.703, p = 0.48; quadratic term Julian²: t =  − 0.736, p = 0.46; scrubjay identity inserted as a random effect). We found no difference in the mean day-to-day mass fluctuation (Fig. 3) or the amplitude of mass fluctuations between females, males, and helpers (F_2,355 = 0.28, p = 0.76; F_2,355 = 1.27, p = 0.28; respectively).

Day-to-day mass fluctuation did not vary by fortnight for females (five fortnights: F_4,62 = 0.57, p = 0.68) and helpers (F_4,80 = 0.70, p = 0.59; Supplemental Information 1). Day-to-day mass fluctuations varied for males (F_4,201 = 2.46, p = 0.05), but only the first (April 1–15; $\bar{x}=-0.58\pm 0.42$ SD) and last (June 1–15; $\bar{x}=0.60\pm 0.19$ SD) fortnights were significantly different (Tukey’s multiple comparisons, p = 0.03). The amplitude of mass fluctuations did not vary by fortnight for females (F_4,62 = 0.73, p = 0.58), males (F_4,201 = 1.09, p = 0.36) or helpers (F_4,80 = 1.17, p = 0.33; Supplemental Information 2). Day-to-day mass fluctuation did not differ between breeding stages (four stages: χ² = 1.39, p = 0.22), for females (χ² = 6.41, p = 0.09), males (χ² = 3.56, p = 0.31) or helpers (F_3,77 = 2.31, p = 0.08; Supplemental Information 1). The amplitude of mass fluctuations did not vary by breeding stage for helpers (F_3,77 = 0.13, p = 0.95). However, the amplitude of mass fluctuations was significantly higher for both females (χ² = 8.32, p = 0.04) and males (F_3,176 = 4.75, p = 0.003) during the building stage than for any other breeding stage (Tukey’s test, p < 0.05 for all comparisons, Supplemental Information 2).

Day-to-day fluctuation in mass of a scrub-jay was positively associated with the maximum temperature on the first day of weighing, as well as with maximum temperature of the first and second days of weighing (Table 2). Day-to-day fluctuation in mass was not associated with minimum temperatures, nor with rainfall. A multivariate analysis of all climatic variables and period of the breeding cycle or class (female breeder, male breeder, or helper) resulted in a final model including only the two maximum temperature values. This result was consistent with findings from the single-factor correlations.

Regulation of body mass

Day-to-day mass fluctuation influenced mass fluctuation between the second and third consecutive days (F_1,236 = 22.2, p < 0.001, $r_{\mathrm{adj.}}^2=0.082$). Usually the mass fluctuation from the second to third day was compensatory (Fig. 4A); however, the influence had only an immediate, short-term effect, and disappeared by the fourth consecutive day (Fig. 4B; F_1,129 = 0.2, p = 0.65, $r_{\mathrm{adj.}}^2=-0.006$). The effect of day-to-day mass fluctuation on mass fluctuation between the second and third days was significant for all classes: female breeders (F_1,44 = 7.81, p = 0.008, $r_{\mathrm{adj.}}^2=0.131$), male breeders (F_1,142 = 7.65, p = 0.006, $r_{\mathrm{adj.}}^2=0.044$), and helpers (F_1,45 = 5.46, p = 0.02, $r_{\mathrm{adj.}}^2=0.088$). Mixed-effect models with serial correlation showed that mass fluctuations over three-day series (t =  − 0.658, p = 0.51) did not differ from those over a four-day series (t =  − 0.835, p = 0.40); Supplemental Information 3).

Temporal patterns of mass variation

Florida scrub-jays exhibited a pattern of diurnal mass gain frequently observed in other diurnal birds (reviewed in Clark Jr, 1979; Haftorn, 1989; Ekman & Lilliendahl, 1993; but see Manu & Cresswell, 2013). Birds weighed the least in the morning, presumable because of nighttime fasting, and gained weight throughout the day. Birds in all social classes—female and male breeders and helpers—exhibited this pattern, although only one helper was measured multiple times within a single day. The 0.205 g gain in mass per hr is great enough to warrant caution whenever mass measurements taken at different times of day are compared. In this study we accordingly inserted the time of the day in all models comparing mass measurements. Time-adjusted measurements of the same birds taken on consecutive days, possible in this study because individuals were trained to land on an electronic balance and therefore were measured without capture are a useful alternative to repeated measurements of birds at the same time of day, for example dawn or dusk, employed in many laboratory studies (e.g., Thomas, 2000), but very difficult to obtain and very stressful for free-living birds (Carpenter, Paton & Hixon, 1983; MacLeod et al., 2005; MacLeod & Gosler, 2006; Moiron, Mathot & Dingemanse, 2018).

Breeding stage and calendar date (fortnights) affected the mass of female breeders. Females exhibited the common pattern in passerines of mass loss between the incubation and nestling stages (reviewed in Moreno, 1989). Mass during the fledgling stage also was lower than mass during the incubation stage. Male breeders did not show a tendency to decrease in mass during the breeding period. Their weigh fluctuated and showed some significant difference when comparing different stages or fortnights, but the differences were small (<1 g). The patterns of mass variation for female and male breeders in this study are consistent with mass data for an adjacent study population of the Florida scrub-jay collected over three years during the building, incubation and nestling stages (Schoech, 1998) and to data collected in the same population in different years (Brand & Bowman, 2012). However, in these studies the patterns of mass variation in helpers were never examined in detail before. Helpers exhibited an increase of mass in the last part of the breeding period, which is somewhat surprising given their energetically demanding contributions to feeding of nestlings (Stallcup & Woolfenden, 1978) and fledglings (McGowan & Woolfenden, 1990). This suggests helpers may be employing a bet hedging strategy by providing help to their parents thereby increasing their indirect fitness, yet at the same time attempting to maintain or even gain mass thereby not potentially reducing their longer-term survival prospects. Several studies documented costs associated with helping in cooperative breeders (Reyer, 1984; Heinsohn & Cockburn, 1994; MacLeod & Clutton-Brock, 2015). Florida scrub-jay helpers might be attempting to minimizing these costs to protect their long-term direct fitness potential by surviving to become breeders.

Day-to-day fluctuations in mass

Day-to-day fluctuations in mass might be stochastic variation or might reflect difficulty in maintaining body mass, such as during unfavorable foraging conditions, cold weather, or a period of elevated energy expenditure. Consistent with the relative stability of Florida scrub-jays’ average mass during this study, most day-to-day fluctuations in mass were small, and overall did not vary between male breeders, female breeders and helpers despite their different breeding-season activities. Mass fluctuations varied significantly relative to season only for male breeders, and only between two fortnights, but these differences were small (−0.58 g during the first fortnight compared to 0.60 g during the last fortnight) and were not reflected by differences in average mass of males between fortnights. Also, the amplitude of mass fluctuations did not vary by fortnight.

In Florida scrub-jays, female breeders perform all incubating and brooding, but feed nestlings at a relatively low rate compared to the male breeder. Male breeders feed the female during incubation and brooding, and feed nestlings at a high rate. Both males and females feed fledglings at an increasing rate that peaks about two weeks post-fledging (Woolfenden & Fitzpatrick, 1996; Stallcup & Woolfenden, 1978; McGowan & Woolfenden, 1990). We found that despite the different reproductive activities of Florida scrub-jays, day-to-day mass fluctuations did not differ among social classes in different stages of the breeding cycle. The amplitude of these fluctuations also did not differ between classes. However, the amplitude of mass fluctuations was higher for female and male breeders during the building stage than during any other stage. The building stage encompassed the prelaying period, so the large amplitude of mass fluctuations for females likely reflects mass gain during the building stage. The average amplitude and fluctuation are equal for this stage, indicating that all fluctuation measurements were positive. The larger amplitude for males during the building stage is more difficult to explain. The average fluctuation for this stage was smaller than the average amplitude, though it was still positive, indicating that day-to-day mass gains were partly offset by losses. No differences in amplitude existed for helpers.

Weather variables explained less than 2% of the total variation in day-to-day mass fluctuation. The lack of effect of daily minimum temperature on mass fluctuation suggests that during the study period the nocturnal energy expenditure of jays was not influenced by nighttime temperature. It is not surprising that Florida scrub-jays in the subtropical climate of south-central Florida, particularly in the spring months of April, May and June, would not exhibit fat storage patterns observed in birds that experience colder temperatures (e.g., Rogers, 1987; Rogers & Smith, 1993; review in Witter & Cuthill, 1993).

Regulation of body mass

Day-to-day mass fluctuation explained 8% of the variation in mass on the third consecutive day. Female breeders, male breeders and helpers exhibited similar short-term mass regulation, with the effect strongest in female breeders (13% of variation explained). Small mass fluctuations over two days, combined with the ability to compensate for these fluctuations on the third day, indicate that during the breeding season scrub-jays are able to regulate their body mass on a short-term basis. A number of studies have found differences in mass regulation strategies between dominant and subordinate birds (Krams, 2000; Krams, 2002). Theory predicts that subordinates should carry greater fat reserves than dominants (Clark & Ekman, 1995; Gosler, 1996; Ratikainen & Wright, 2013) as insurance against poor foraging conditions, during which dominants would exercise their priority access to food. Some studies have found that the body mass of subordinates varies less than that of dominants, likely because smaller adjustments are needed to subordinates’ already larger reserves (in Willow Tits Parus montanus, Ekman & Lilliendahl, 1993; Great Tits Parus major, Gosler, 1996; and Greenfinches Carduelis chloris, Hake, 1996; but the opposite result in Coal Tits Parus ater, Polo & Bautista, 2002). In contrast, in Florida scrub-jays, although helpers are subordinate to male breeders, they exhibited similar day-to-day mass fluctuations, amplitude of fluctuations and short-term mass regulation. These previous studies were performed on dominance-structured winter flocks of genetically unrelated individuals in which dominants were able to monopolize food resources, leading to different strategies. In Florida scrub-jays, dominant and subordinate birds within groups are closely related. Jays tend to forage individually primarily on insects and, to a lesser extent, small reptiles, amphibians, and mammals all well hidden in the vegetation. This reduces the chance for dominant birds to monopolize food. In fall and winter, each jay feeds primarily on acorns, cached during the later summer. Each jay scatter-hoards 6-7000 individual acorns (DeGange et al., 1989). When caching, jays adopt behaviors that appear to minimize kelptoparsitism by dominant jays, suggesting that it may happen but is minimized within groups (Toomey, Bowman & Woolfenden, 2007). Thus year-round feeding patterns do not favor despotic control of food. Since breeder and helper jays both contribute to rearing young, it is not surprising that in this species, mass regulation strategies did not differ by social status.

Because the jays rarely experience severe climate or food shortages in spring (Woolfenden & Fitzpatrick, 1996), a strategy of fattening may be more of a disadvantage (Lima, 1986) than an advantage. Instead, for this species, the appropriate strategy seems to be maintain a stable body mass that effectively balance the need to maintain some energy reserves against the need for efficient flight and foraging, as required during reproduction.