Seasonal Interactions Between Photoperiod and Maternal Effects Determine Offspring Phenotype in Franklin’S Gull

Functional Ecology 2012, 26, 948–958 doi: 10.1111/j.1365-2435.2012.02010.x Seasonal interactions between photoperiod and maternal effects determine offspring phenotype in Franklin’s gull

Mark E. Clark* and Wendy L. Reed

Department of Biological Sciences, North Dakota State University, P.O. Box 6050, Dept. 2715, Fargo, North Dakota, 58108-6050 USA

Summary 1. When predictable seasonal changes affect offspring fitness, we expect offspring to evolve phenotypes that minimize the costs of seasonal variation in timing of breeding. For species with parental care during embryonic development, offspring receive seasonal cues of the environment from parents that are biased by their parent’s fitness (which is not equivalent to offspring fitness). Therefore, mechanisms enabling offspring to detect environmental cues independent of parents should be strongly favoured. 2. We experimentally evaluated the ability of avian embryos to integrate cues of season from photoperiod and maternal environments present in eggs to produce seasonal variation in phenotypes among Franklin’s gull (Leucophaeus pipixcan) hatchlings. Eggs were collected early and late in the season and some were separated into their component parts and others were incubated under short (early season) and long (late season) photoperiods. After hatching, we measured the structural size of the chicks and the amount of yolk sac reserves. 3. We found that hatchling size, a phenotype linked with fitness, is sensitive to both egg con- tents provided by mothers and photoperiod, and development time decreases across the season. The effects of integrating cues of season from eggs and photoperiod on offspring phenotype are complex, and when cues of season from eggs are mismatched with cues of season from photoperiod, alternate phenotypes are created. 4. We also found that seasonal variation in egg size, yolk, albumen or shell content of the eggs do not account for the seasonal maternal egg effect on hatchling size. This seasonal maternal effect could be a result of other egg constituents or reflect heritable variation in timing of breeding that is linked with offspring size. 5. Changes in breeding phenology of adults could result in a mismatch between cues from parents and photoperiod cues of season. For example, if breeding seasons advanced such that late season birds initiate breeding at an early season photoperiod, offspring would then be integrating maternal cues of late season with photoperiod cues of early season and alter their phenotypes. We expect our results to initiate new studies on how vertebrate embryos integrate environmental cues with maternal effects and offspring responses to optimize the expression of offspring phenotype.

Key-words: avian, embryonic development, Leucophaeus pipixcan, life-history trade-offs, parent–offspring conflict, phenotypic plasticity, photoperiodism, seasonality

organisms (Bradshaw & Holzapfel 2007). In temperate Introduction regions, seasonal increases in temperature, water and Animals exploiting seasonal environments take advantage energy provide times for which ﬁtness is maximized by of regular changes in resources, which are responsible for reproduction and rearing young, whereas decreases in these organizing biological processes and the annual cycle of resources result in times when ﬁtness is maximized by migration or quiescent life-history phases. The ability to *Correspondence author. E-mail: [email protected] predict seasonal changes correctly and initiate appropriate

© 2012 The Authors. Functional Ecology © 2012 British Ecological Society Seasonal effects on offspring phenotype 949 behavioural, physiological and biochemical responses that have a higher likelihood of survival than offspring pro- maximize fitness is shaped by natural selection (Bradshaw duced late in the season (Moreno 1998; Drent 2006; Ver- & Holzapfel 2007; Lyon, Chaine & Winkler 2008). Photo- hulst & Nilsson 2008). Parents are predicted to favour period provides a consistent cue of season that animals use offspring with higher likelihood of survival, especially to predict optimal timing for annual events (Bradshaw & when allocation of resources to offspring with low likeli- Holzapfel 2007; Lyon, Chaine & Winkler 2008), and the hood of survival decreases future reproductive potential of refinement of timing of breeding within a season is pro- parents [i.e. the reproductive constraint hypothesis (Win- vided by additional biotic and abiotic cues (Wingfield & kler 1987; Stearns 1992; Verhulst & Nilsson 2008)]. The Kenagy 1991; Visser, Holleman & Caro 2009; Visser et al. consequences of seasonal variation in reproduction have 2011). The influence of photoperiod in orchestrating sea- been considered mainly from the perspective of conse- sonal changes in adult phenotype has a long history of quences for parental fitness and trade-offs between current study, but the influence of photoperiod and season on juve- and future offspring. In seasonal environments, parents nile phenotype has been little explored outside invertebrate must transition from breeding to preparation for migration systems (Dmitriew 2011). and winter. Offspring and parental fitness, however, are A rich body of literature documents the influence of sea- not equivalent (Wolf & Wade 2001; Mu¨ller et al. 2007) son and photoperiod on producing adaptive phenotypes in and the consequences of season on current offspring fitness juvenile and larval invertebrates (Kingsolver & Huey 1998; are large. Offspring are under similar seasonal time con- Bradshaw & Holzapfel 2010; Sniegula & Johansson 2010; straints as adults as well as additional constraints; that is, Beldade, Mateus & Keller 2011). However, the life histo- they must grow, develop and moult, as well as learn to for- ries of many of these invertebrates (i.e. mosquitos, pea age and fly to be ready to migrate. When the costs of sea- aphids and butterflies) do not include parental care. In the sonal timing are high for offspring, we expect offspring to absence of parental care, juveniles interact directly with evolve mechanisms to detect timing of season, and mecha- their environments, which minimizes any conflict between nisms to mitigate negative fitness consequences of seasonal offspring and parent because the offspring phenotype is variation in timing of breeding. unlikely to affect future reproductive success of parents. In Examining the effect of seasonality on offspring fitness is contrast, when parents provide prenatal or natal care, particularly relevant in birds, which have served as a criti- embryos and juveniles experience environments as trans- cal model and indicator of shifts in timing of seasonal lated by or through parents and the offspring phenotype events (Lyon, Chaine & Winkler 2008). Consistent changes can directly affect future reproductive success of parents. in temperatures across local and global scales are affecting For example in mammals, photoperiods experienced by annual cycles of plants and animals (Bradshaw & Holzap- females can be translated to their foetuses through changes fel 2008); however, photoperiod is not labile. The extent to in maternal hormones, resulting in long-term effects on off- which a mismatch between photoperiodic cues of season spring life-history traits (Horton 2005) and adult condition and temperature driven changes in seasonality affects bio- (French et al. 2009). Such maternal effects are also present logical systems requires knowledge of the mechanisms by in oviparous animals, although direct exchange of mater- which organisms sense and respond to seasonal environ- nal resources with offspring is limited to a short period of ments. Avian embryos are capable of sensing and respond- time prior to oviposition (Schwabl 1996b; Groothuis & ing to photoperiod as demonstrated in poultry (Siegel Schwabl 2008). Bird eggs contain maternally derived et al. 1969b; Shafey 2004a), but has only recently been androgens (Reed & Vleck 2001; Groothuis et al. 2005; explored as an adaptive mechanism affecting incubation Boonstra, Clark & Reed 2009), melatonin (Bozenna et al. period in wild populations (Cooper et al. 2011). Current 2007), thyroid hormones (Wilson & McNabb 1997), anti- hypotheses of photoperiod effects on avian embryonic bodies (Grindstaff, Brodie & Ketterson 2003), carotenoids development focus on the function of day length in setting (Newbrey & Reed 2009), vitamins (Biard et al. 2009) and the circadian rhythm in the final stages of incubation RNA transcripts (Knepper et al. 1999; Malewska & Ols- (Nichelmann, Hochel & Tzschentke 1999; Okabayashi zanska 1999), all of which are biologically active, poten- et al. 2003), photo acceleration of development (reviewed tially affect embryonic growth and development and can in Cooper et al. 2011; and Reed & Clark 2011) and photo- vary seasonally (Watanabe et al. 2007; Hargitai et al. periodic effects on post-hatching growth in artificially 2009). Although birds have played a critical role in evalu- incubated poultry (Rozenboim et al. 2003). ating both the impacts of maternal provisioning on off- Under the reproductive constraint hypothesis, animals spring (Groothuis et al. 2005) and changes in adult that are long-lived, undergo long migrations and provide phenology in response to changing seasons (Lack 1950; parental care are expected to invest more in their own sur- Perrins 1970), the ability of avian embryos to integrate vival at a cost to their current offspring when those off- both maternal and photoperiod cues of season has not spring have a low probability of survival (Winkler 1987; been explored. Stearns 1992). Gulls and other seabirds have high adult One consequence of seasonal environments is variation survivorship, make long migrations, provide significant in reproductive value of offspring across the season. Off- parental care to their chicks and exhibit seasonal declines spring produced at the beginning of the season typically in fecundity and reproductive success (Moreno 1998) as

© 2012 The Authors. Functional Ecology © 2012 British Ecological Society, Functional Ecology, 26, 948–958 950 M. E. Clark & W. L. Reed expected by the reproductive constraint hypothesis. These that the observed seasonal variation in tarsus length at characteristics make them particularly good models to hatch resulted from seasonal effects of either photoperiod evaluate our hypothesis that offspring are able to alter or maternal egg composition on embryonic development. development in response to seasonal cues obtained inde- We tested our hypotheses by experimentally controlling pendent of parents, which has not been well documented day length for artificially incubated Franklin’s gull eggs in free-living populations. collected both during the early and late stages of the nest- In a wild population of Franklin’s gull (Leucophaeus ing season. To understand how maternal investments vary pipixcan), we observed systematic changes in hatchling size with season, we characterized maternal investments in egg as the breeding season progressed (Fig. 1). In this popula- size, yolk, albumen and eggshell across the season. To tion, late season hatchlings had shorter tarsi than early evaluate whether or not embryos were using egg resources season hatchlings (Fig. 1a), but this pattern was not differently across the season, we evaluated the effects of explained by smaller hatchling mass (Fig. 1b). These treatments on hatchling composition (carcass mass and observations were unique because absolute mass at hatch residual yolk-sac mass). did not change across the season; yet structural size at hatch (i.e. tarsus length) did change with season. More- Materials and methods over, hatchling size and hatch date were related to observed differences in growth and survival (Berg 2009). FIELD OBSERVATIONS Seasonal variation in structural size at hatch suggests that the way in which offspring grow and develop varies across Observational data on tarsus length of newly hatched chicks were the season, with consequences for fitness. We hypothesized collected as part of a previous study on chick survival (Berg 2009). Briefly, Berg (2009) visited nests to determine hatch dates and measure chicks at hatching in a Franklin’s gull colony at J. Clark Salyer National Wildlife Refuge (NWR), which is located along the Souris river in north-central North Dakota, USA. Eggs in (a) nests were marked with a unique code, and nests were checked daily for evidence of pipping (the onset of hatching) eggs near the estimated hatch dates. Within 12 h of hatching, hatchling mass (±0·5 g) and right tarsus (±0·1 mm) were measured and the hatchling was returned to the nest. Franklin’s gulls hatch asynchro- nously (Burger & Gochfeld 1994), and the first hatchling in each nest was the only one measured from the nest.

EXPERIMENTAL EGG INCUBATION

To test our hypotheses about the factors affecting embryonic development, we collected freshly laid eggs between May 7 and June 10, 2009, at two field sites in north-central North Dakota (J. Clark Salyer NWR and Lake Alice NWR). We collected eggs from the beginning (May 7 at J. Clark Salyer and May 27 at Lake Alice) and at end of the nest initiation period (June 3 at J. Clark (b) Salyer and June 10 at Lake Alice) and artificially incubated them in the laboratory. We determined whether eggs were freshly laid by (i) collecting eggs from nests only containing single eggs, (ii) checking eggs for incubation by touch (feeling eggs for warmth) and (iii) by floating eggs (Nol & Blokpoel 1983; Ackerman & Eagles-Smith 2010). We collected the first-laid egg in nests on a single day within the first week nesting was observed (i.e. early season) and on a single day approximately 3 weeks later, at which point approximately 80% of nests had been initiated (i.e. late season) in the 2009 breeding season at J. Clark Salyer NWR and Lake Alice NWR. We measured length (±0·1 mm) and breadth (±0·1 mm) and brought the eggs to our laboratory within 8 h of collection for either artificial incubation under experimental day length treatments, or dissection to determine egg composition. We randomly assigned each egg to a short (14 : 10 light : dark cycle) or long (18 : 6 light : dark cycle) day length treatment during incubation, or to a group that would be dissected for determination of egg composition (yolk, albumen and eggshell). Eggs in the incubation treatments were assigned to one of four incubators Fig. 1. (a) Tarsus length at hatching (filled circles) declines signifi- maintained at 37·5 °C and 65% relative humidity. Incubators had 2 cantly with hatch day (F1,45 = 17·36, P < 0·001, r = 0·28, n = 47; large, insulated plexi-glass windows and automatic egg turners solid line) but (b) mass at hatching (filled circles) does not change (Hova-Bator 1586 Picture Window incubator). 2 with hatch day (F1,45 = 1·67, P = 0·203, r = 0·04, n = 47; solid Incubators were placed inside environmental chambers that line) in Franklin’s gull chicks. maintained a constant temperature (24 °C), relative humidity

(40%) and differed only by the assigned photoperiod. Both envi- measurements for two of the 12 hatchlings from the late ronmental chambers were equipped with full-spectrum light bulbs season long day length group were missing. set to timers. One chamber maintained a short day length (14 : 10 light : dark cycle) that mimicked an early season photoperiod, and the other chamber maintained a long day length(18 : 6 HATCHLING SIZE light : dark cycle) that mimicked a late season photoperiod typical for latitudes where Franklin’s gulls nest. In each chamber, a bank The full model for tarsus length at hatching explained a of four full-spectrum bulbs was placed approximately 25 cm significant amount of variation (n = 61, F7,53 = 5·96, above each incubator. Incubators were thus subjected to a photo- P < 0·001, r2 = 0·44), with significant effects as a result of period/chamber treatment; however, we refer to this as a photoperiod treatment henceforth. After 21 days of incubation, we season (i.e. smaller tarsi in hatchlings from late season 2 removed eggs from the automatic turners, checked the eggs daily eggs; F1,53 = 4·44, P = 0·040, r = 0·05), photoperiod (i.e. for evidence of hatching, collected freshly hatched (i.e. within 6 h smaller tarsi in hatchlings from eggs incubated with longer of hatching) chicks and recorded time to hatching (in days). Time 2 day lengths; F1,53 = 11·29, P = 0·002, r = 0·12), incubator to hatching was measured as the number of days elapsed between nested within photoperiod treatment (F = 5·16, the day eggs were placed in incubators to the day that they 2,53 = · 2 = · hatched. We measured mass (±0·01 g) and right tarsus (±0·1 mm) P 0 009, r 0 11) and egg mass (i.e. longer tarsi in of hatchlings, and dissected a subset to determine mass (±0·01 g) hatchlings from larger eggs; F1,53 = 7·32, P = 0·029, of the residual yolk sac and yolk-free carcass after drying (at r2 = 0·08) (Fig. 2), but no significant interaction between 40 °C) to a constant mass. 2 season and photoperiod (F1,53 = 1·30, P = 0·260, r = 0·01) 2 or location (F1,53 = 1·45, P = 0·234, r = 0·02) (Table 1). EGG COMPOSITION When we included all 79 hatchlings (and therefore removed the egg mass term), the model explained a signifi- Eggs assigned to dissection were weighed, gross components (i.e. cant amount of variation in tarsus length (F = 4·14, shell, albumen and yolk) separated and weighed, then dried and 6,72 = · 2 = · reweighed. We measured mass (±0·001 g) of the whole egg on a P 0 001, r 0 26), and still had significant effects of digital balance, and carefully opened each egg with scissors to sep- season (i.e. smaller tarsi in hatchlings from late season ° 2 arate shell, albumen and yolk. We then dried (40 C) the compo- eggs; F1,72 = 8·59, P = 0·005, r = 0·09), photoperiod (i.e. nents to a constant (dry) mass (±0·001 g). smaller tarsi in hatchlings from eggs incubated with longer 2 day lengths; F1,72 = 12·24, P = 0·001, r = 0·13) and incu-

STATISTICAL ANALYSES bator nested within photoperiod treatment (F2,72 = 3·14, P = 0·049, r2 = 0·06) (Table 1). There were no differences We used nested general linear models to analyse hatchling charac- in tarsus length between early season eggs receiving short teristics and egg composition statistically. For tarsus size, hatch- = · = · ling mass, hatchling composition and incubation time, we or long day length photoperiod cues (t 1 69, P 0 097), included terms for season (early vs. late), photoperiod (14 h vs. but late season eggs receiving short day length photoperi- 18 h day length), egg mass (estimated fresh egg mass based on ods had longer tarsi at hatching than late season eggs · · 0·78 · 2·04 0 0011 length breadth from Berg (2009)), collection loca- receiving long day length photoperiod (t = 3·11, tion (J. Clark Salyer vs. Lake Alice) as a random effect, incubator nested within photoperiod treatment and an interaction between season and photoperiod. A post-hoc student t-test was used to compare least-square means among season 9 photoperiod groups to compare phenotypes created under matched cues of season to phenotypes created from mismatched cues. For models of egg composition, we included terms for season, collection location (henceforth location) and an interaction between season and location. For all models, Shapiro–Wilk tests indicated that residuals were normally distributed. Significance was based on a = 0·05.

Results We collected 120 eggs and assigned them to incubators (30 per incubator, with 15 from early season nests and 15 from late season nests). A total of 79 hatched (21 from the early season short day length group, 21 from the early season long day length group, 24 from the late season short day Fig. 2. Tarsus length at hatching (least square means ±95% confi- length group and 13 from the late season, long day length dence interval) from eggs laid early and late in the season that group) and we had estimates of egg mass for 61 of these were artificially incubated under experimental photoperiod treat- eggs (21 from the early season, short day length group, 13 ments (14 : 10 vs. 18 : 6 light : dark 24-h cycle) varied signifi- = · < · 2 = · from the early season long day length group, 15 from the cantly (F7,53 5 96, P 0 001, r 0 44), with effects as a result 2 of season (F1,53 = 4·44, P = 0·040, r = 0·05), photoperiod late season short day length group and 12 from the late 2 (F1,53 = 11·29, P = 0·002, r = 0·12), incubator (F2,53 = 5·16, season, long day length group). Hatchling mass measure- 2 P = 0·009, r = 0·11) and egg mass (F1,53 = 7·32, P = 0·029, ments were available for 59 of the 61 hatchlings for which r2 = 0·08). Differences among treatments (a, b) and sample sizes egg mass estimates were available because hatching mass (n) are indicated above each confidence interval.

Table 1. General linear modelling results for hatchling size, composition and time to hatch. Sample size (n), F statistic value (F), P value (P) and coeﬃcient of determination (R2) for the full general linear models (with 9 indicating interaction and [] indicating a nested eﬀect) as well as respective individual model terms (shown in italics). Power (Power) is reported only for individual categorical variables. The number of levels for each categorical variable is also listed in the sample size column

Model nF P R2 Power

Tarsus = Season + Photo + Season 9 Photo + Inc[Photo] + Loc + Emass 61 5·96 <0·001 0·44 Season 24·44 0·040 0·05 0·54 Photo 211·29 0·002 0·12 0·91 Season 9 Photo 41·30 0·260 0·01 0·20 Inc [Photo] 45·16 0·009 0·11 0·81 Loc 21·45 0·234 0·02 0·22 Emass 7·32 0·029 0·08 Tarsus = Season + Photo + Season 9 Photo + Inc[Photo] + Loc 79 4·14 0·001 0·26 Season 28·59 0·005 0·09 0·82 Photo 212·24 0·001 0·13 0·93 Season 9 Photo 40·68 0·411 0·01 0·13 Inc [Photo] 43·14 0·049 0·06 0·59 Loc 20·56 0·456 0·01 0·11 Chick mass = Season + Photo + Season 9 Photo + Inc[Photo] + Loc + Emass 59 10·51 <0·001 0·59 Season 20·06 0·816 0·00 0·06 Photo 23·74 0·059 0·03 0·48 Season 9 Photo 40·06 0·813 0·00 0·06 Inc[Photo] 42·43 0·098 0·04 0·47 Loc 211·24 0·002 0·09 0·91 Emass 42·63 <0·001 0·34 Residual YS = Season + Photo + Season 9 Photo + Inc[Photo] + Loc + Emass 24 5·00 0·004 0·69 Season 213·32 0·002 0·26 0·93 Photo 219·19 0·001 0·38 0·98 Season 9 Photo 46·53 0·021 0·13 0·67 Inc[Photo] 43·83 0·044 0·15 0·61 Loc 2 <0·01 0·955 0·00 0·05 Emass <0·01 0·995 0·00 Residual YS = Season + Photo + Season 9 Photo + Inc[Photo] + Loc 40 2·12 0·077 0·28 Season 24·45 0·043 0·10 0·54 Photo 25·15 0·030 0·11 0·60 Season 9 Photo 40·76 0·388 0·02 0·14 Inc[Photo] 40·03 0·967 0·00 0·05 Loc 2 <0·01 0·962 0·00 0·05 Yolk free carcass = Season + Photo + Season 9 Photo + Inc[Photo] + Loc + Emass 23 2·70 0·051 0·56 Season 22·94 0·107 0·09 0·36 Photo 23·05 0·101 0·09 0·37 Season 9 Photo 40·46 0·506 0·01 0·10 Inc[Photo] 41·16 0·339 0·07 0·22 Loc 21·00 0·332 0·03 0·16 Emass 6·49 0·022 0·19 Time to hatch = Season + Photo + Season 9 Photo + Inc[Photo] + Loc + Emass 42 2·74 0·023 0·36 Season 24·84 0·035 0·09 0·57 Photo 23·59 0·067 0·07 0·45 Season 9 Photo 40·62 0·438 0·01 0·12 Inc[Photo] 41·48 0·243 0·06 0·29 Loc 22·19 0·148 0·04 0·30 Emass 1·13 0·295 0·02 Time to hatch = Season + Photo + Season 9 Photo + Inc[Photo] + Loc 49 2·45 0·040 0·26 Season 26·88 0·012 0·12 0·73 Photo 20·42 0·520 0·01 0·10 Season 9 Photo 43·28 0·077 0·06 0·42 Inc[Photo] 40·53 0·592 0·02 0·13 Loc 21·19 0·281 0·02 0·19

2 P = 0·003) (Fig. 2). In contrast to tarsus length, hatchling son (F1,51 = 0·06, P = 0·816, r < 0·01), photoperiod 2 2 mass (full model F7,51 = 10·51, P < 0·001, r = 0·59) was (F1,51 = 3·74, P = 0·059, r = 0·03), the interaction between 2 aﬀected by egg mass (i.e. larger hatchlings hatched from photoperiod and season (F1,51 = 0·06, P = 0·813, r < 0·01) 2 larger eggs; F1,51 = 42·63, P < 0·001, r = 0·34) and loca- or incubator nested within photoperiod treatment 2 2 tion (F1,52 = 11·24, P = 0·002, r = 0·09), but not by sea- (F2,51 = 2·43, P = 0·098, r = 0·04) (Table 1).

2 = · HATCHLING COMPOSITION r 0 11). The full model for yolk-free dry carcass mass at hatching did not explain a significant amount of variation 2 We determined body composition (i.e. dry residual yolk (F7,15 = 2·70, P = 0·051, r = 0·56), but was positively sac mass and dry yolk-free carcass mass) for a subset of 40 affected by egg mass (i.e. greater yolk-free carcass mass of hatchlings (nine from the early season, short day length hatchlings from larger eggs; F1,15 = 6·49, P = 0·022, group, nine from the early season, long day length group, r2 = 0·19) (Table 1) and power was limited (Table 1). 15 from the late season, short day length group and seven Early season eggs receiving a long day length photoperiod from the late season, long day length group), and 24 had cue hatched with more residual yolk sac than early season estimates of egg mass (nine from the early season, short eggs receiving short day length photoperiod cues (t = 4·14, day length group, two from the early season, long day P = 0·001) (Fig. 3). In contrast, there were no differences length group, seven from the late season, short day length in yolk sac reserves between late season eggs receiving group and six from the late season, long day length short or long day length photoperiods (t = 1·71, group). Yolk-free carcass mass was not available for one P = 0·108). of the nine early season, short day length hatchlings that had estimates of egg mass. The full model explained a sig- EGG COMPOSITION nificant amount of the variation in dry yolk sac mass 2 (F7,16 = 5·00, P = 0·004, r = 0·69; Fig. 3) with a signifi- We determined gross egg components (i.e. egg mass, dry cant negative effect of season (i.e. smaller residual yolk sac yolk mass, dry albumen mass and dry eggshell mass) for in hatchlings from late season eggs; F1,16 = 13·32, 45 freshly laid Franklin’s gull eggs (18 early season and six 2 P = 0·002, r = 0·26), positive effect of photoperiod (i.e. late season eggs from J. Clark Salyer NWR, and 14 early greater residual yolk sac in hatchlings from eggs incubated season and seven late season eggs from Lake Alice NWR). = · = · under longer day lengths; F1,16 19 19, P 0 001, There were no differences in egg mass (F3,41 = 1·27, 2 = · 2 r 0 38), an interaction between season and photoperiod P = 0·300, r = 0·09), dry yolk mass (F3,41 = 1·83, = · = · 2 = · 2 (F1,16 6 53, P 0 021, r 0 13), and an effect of incu- P = 0·156, r = 0·12), dry albumen mass (F3,41 = 1·10, = · 2 bator nested within photoperiod treatment (F2,16 3 83, P = 0·359, r = 0·07) or dry eggshell mass (F3,41 = 1·19, P = 0·044, r2 = 0·15) (Table 1). Effects of location P = 0·324, r2 = 0·08) associated with season or location 2 (F1,16 < 0·01, P = 0·955, r < 0·01) and egg mass(F1,16 < (Table 2). 0·01, P = 0·995, r2 < 0·01) were not significant (Table 1). When all dry yolk sac masses were included (and thus the egg mass term removed), the full model did not explain a Table 2. General linear modelling results for egg composition. significant amount of variation (F = 2·12, P = 0·077, Sample size (n), F statistic value (F), P value (P) and coefficient of 6,33 determination (R2) for the full general linear models (with 9 indi- 2 = · r 0 28) (Table 1), but there were still significant negative cating interaction) as well as respective individual model terms 2 effects of season (F1,33 = 4·45, P = 0·043, r = 0·10) and (shown in italics). Power (Power) is reported only for individual positive effects of photoperiod (F1,33 = 5·15, P = 0·030, categorical variables. The number of levels for each categorical variable is also listed in the sample size column

Model nF P R2 Power

Egg mass = Season + Loc + 45 1·27 0·300 0·09 Season 9 Loc Season 23·05 0·088 0·07 0·40 Loc 20·43 0·514 0·01 0·10 Season 9 Loc 40·36 0·550 0·01 0·09 Yolk 45 1·83 0·156 0·12 mass = Season + Loc + Season 9 Loc Season 20·18 0·675 <0·01 0·07 Loc 20·90 0·348 0·02 0·15 Season 9 Loc 42·20 0·145 0·05 0·31 Albumen 45 1·10 0·359 0·07 mass = Season + Loc + Season 9 Loc Season 23·15 0·083 0·07 0·41 Fig. 3. Residual yolk sac mass at hatching (least square means Loc 20·04 0·852 <0·01 0·05 ±95% confidence interval) from eggs laid early and late in the sea- Season 9 Loc 4 <0·01 0·959 <0·01 0·06 son that were artificially incubated under experimental photope- Shell 45 1·19 0·324 0·08 riod treatments (14 : 10 vs. 18 : 6 light : dark 24-h cycle) varied mass = Season + Loc + = · = · 2 = · significantly (F7,16 5 00, P 0 004, r 0 69) with effects of sea- Season 9 Loc = · = · 2 = · son (F1,16 13 32, P 0 002, r 0 26), photoperiod Season 23·27 0·078 0·07 0·42 = · = · 2 = · = · (F1,16 19 19, P 0 001, r 0 38) and incubator (F1,16 3 83, Loc 20·13 0·725 <0·01 0·06 2 P = 0·044, r = 0·15). Differences among treatments (a, b) and Season 9 Loc 40·14 0·709 <0·01 0·07 sample sizes (n) are indicated above each confidence interval.

INCUBATION PERIOD

We were able to determine time (to the nearest day) to hatching for 49 of the hatchlings (16 from the early season short day length group, 17 from the early season long day length group, nine from the late season short day length group and seven from the late season long day length group). Egg mass estimates were available for 42 of these hatchlings (16 from the early season short day length group, 13 from the early season long day length group, six from the late season short day length group and seven from the late season long day length group). Only negative season effects (i.e. shorter time to hatching for late season 2 eggs; F1,34 = 4·84, P = 0·035, r = 0·09) were evident in the model for time to hatching (F7,34 = 2·74, P = 0·023, Fig. 4. Time to hatch (least square means ±95% confidence inter- 2 val) from eggs laid early and late in the season that were artifi- r = 0·36) (Table 1). Negative season effects (F1,42 = 6·88, P = 0·012, r2 = 0·12) were still evident in a reduced model cially incubated under experimental photoperiod treatments 2 (14 : 10 vs. 18 : 6 light : dark 24-h cycle) varied significantly (F6,42 = 2·45, P = 0·040, r = 0·26; Fig. 4) without the egg 2 (F7,34 = 2·74, P = 0·023, r = 0·36) with effects of season 2 mass term, but no other effects were detected (Table 1). (F1,34 = 4·84, P = 0·035, r = 0·09). Differences among treatments Early season eggs receiving a long day length photoperiod (a, b) and sample sizes (n) are indicated above each confidence cue shortened time to hatch relative to early season eggs interval. receiving short day length photoperiod (t = À2·40, P = 0·022), whereas late season eggs receiving short or long day length photoperiods hatched in a similar amount ble for the maternal effect identified in our experiment. of time (t = 0·72, P = 0·474) (Fig. 4). This suggests that maternal investment in egg constituents (e.g. hormones, carotenoids and antibodies) resulting in epigenetic regulation of gene expression(Natt et al. 2009) Discussion provide more likely mechanisms responsible for the mater- We identified effects of both season and photoperiod on nal effect observed in the experiment. Alternatively, the offspring phenotype. Late season eggs produced hatchlings seasonal egg effects could reflect heritable variation for with shorter tarsi than early season eggs (Fig. 2). Similarly, growth, if growth is related to heritable variation in timing long day lengths during incubation resulted in shorter tar- of reproduction like that found in great tits (Parus major) sus length at hatching relative to hatchlings exposed to (Visser et al. 2011). This particular hypothesis warrants short day lengths during incubation (Fig. 2). The main further evaluation and careful study to separate genetic effects of season and photoperiod on tarsus length mimic effects from maternal effects derived from seasonal varia- the seasonal pattern identified in the field (Fig. 1). The tion in phenotype (Kruuk, Merila & Sheldon 2001). Chick effects of season and photoperiod on yolk sac reserves, growth and survival decline with hatch date in this popula- which are a metric of the amount of energy and resources tion (Berg 2009), thus a seasonal change in the quality of used during development, are complex. Early season eggs maternal investments is consistent with the reproductive produce hatchlings with more yolk sack reserves remaining constraint hypothesis and trade-offs between current and after development than hatchlings from late season eggs, future offspring. but hatchlings from eggs exposed to short day lengths have The deposition of steroid hormones and carotenoids in less yolk sac reserves than hatchlings from eggs exposed to avian eggs can vary across the breeding season (Rubolini long day lengths during incubation. These differences may et al. 2006; Saino et al. 2008; Hargitai et al. 2009; Schoech be a result of effects of increased photoperiod on decreas- et al. 2009), which provides a potential mechanism for sea- ing incubation period (Cooper et al. 2011). Collectively, sonal maternal effects. For example testosterone levels in our results indicate that avian embryos are integrating egg yolks are reported to decline with season in several maternal investments and photoperiod cues of season to species of birds (Schwabl 1996a; Pilz et al. 2003; Gil et al. adjust their development and that the phenotypes that 2006; Tobler, Granbom & Sandell 2007), although see arise result from complex interactions between egg Mu¨ller et al. (2004) and Tomita et al. (2011). Moreover, environments and photoperiod. female canaries (Serinus canaria) exposed to long day The effect of mothers (early vs. late season eggs) on tar- lengths produce eggs with lower levels of yolk testosterone sus length and the amount of yolk sac reserves suggests than females exposed to short day lengths (Schwabl that egg components vary across the season and affect off- 1996a). Yolk androgens affect growth in bird embryos spring development (Figs 2 and 3). Female investment in (Schwabl 1996b; Lipar, Ketterson & Nolan 1999; Lipar & egg mass and yolk, albumen and eggshell did not change Ketterson 2000), which is one approach for females to seasonally and, thus, are unlikely the mechanism responsi- manipulate embryonic phenotype across the season. Like-

© 2012 The Authors. Functional Ecology © 2012 British Ecological Society, Functional Ecology, 26, 948–958 Seasonal effects on offspring phenotype 955 wise, carotenoids and antioxidant activity also have been decreased amount of time to hatch for the early season shown to decline across the breeding season (Rubolini hatchlings receiving mismatched cues of day length relative et al. 2006; Saino et al. 2008). Carotenoids are biologically to the early season eggs receiving matched cues of day active compounds that can mitigate oxidative stress and length (Fig. 4). Cooper et al. (2011) also detected a direct enhance immune function in developing embryos (Saino effect of increased photoperiod on shortening development et al. 2003; Rubolini et al. 2006). Changing patterns of time in house sparrows (Passer domesticus), but could not maternal investments in yolk have been interpreted as a test for seasonal egg effects. The pattern we found among decline in female quality across the season, with changes in early season eggs (Fig. 4) was consistent with that of Coo- investments as adaptive strategies for females to allocate per et al. (2011). In contrast, the time to hatch in late sea- resources between current and future offspring, or the son eggs does not appear to be sensitive to photoperiod (i. changes are interpreted as a response to deteriorating e. there was no change in time to hatch in late season eggs environmental quality across the season (Nilsson 1999). exposed to short days). We hypothesize that the seasonal In addition to responding to investments made at the egg effect driving time to hatch in late season eggs over- time eggs are produced (seasonal egg effect), Franklin’s rides any effect of photoperiod, but the same is not true gull embryos are responding directly to cues about the for early season eggs. Our data do indicate that maternal time of season through photoperiod. Embryos exposed to cues (egg constituents) and photoperiod affect the effi- long day lengths hatch with shorter tarsi than embryos ciency and rate of avian embryonic development and that exposed to short day lengths, and the effect on tarsus the embryo itself is integrating these cues in complex ways seems to be driven by late season eggs exposed to long to produce phenotypic characteristics related to fitness photoperiods (Fig. 2). These responses by embryos may be (Kruuk, Merila & Sheldon 2001). adaptive in producing phenotypes that are best matched to Photoperiods provide consistent cues of seasonal varia- early vs. late season growth and survival, which needs to tion in environments, but they also vary consistently across be evaluated in field experiments. When parents vary care latitude. Cooper et al. (2011) interpret changes in develop- for offspring across the season based on the value of cur- mental time as an adaptive response to shorter breeding rent offspring compared to future offspring (Winkler seasons in northern latitudes and partially responsible for 1987), current offspring receive a signal of season biased shorter incubation periods that occur at higher latitudes in by parental fitness. Because of this high level of control, many species (Martin et al. 2007; Robinson et al. 2008). parents can influence offspring phenotypes in a way that Shorter development time late in the season (or at higher benefits their own fitness. However, offspring fitness is not latitudes) could be beneficial for late hatching offspring that equivalent to parental fitness (Wolf & Wade 2001; Mu¨ller are more time constrained than offspring hatching earlier in et al. 2007). Thus, when the cost of seasonality is largely the season (or at lower latitudes). For example common incurred by the offspring, we expect offspring to respond murre (Uria aalge) chicks hatching from late season eggs to cues of season independent of cues provided by parents, have the capacity to grow faster and fledge sooner than and selection to favour offspring phenotypes that mitigate chicks from early season eggs (Benowitz-Fredericks & these costs (Reed & Clark 2011). Therefore, cues of season Kitaysky 2005). The photoperiod effect found in house that are derived independent of parental investment pro- sparrow embryos (Cooper et al. 2011) and our findings in vide offspring with an unbiased signal by which they can Franklin’s gull hatchlings suggest that a single mechanism adjust their phenotype. Our data indicate that avian may be responsible for plasticity in offspring phenotypes embryos do have the ability to sense external environments that occur across seasons as well as latitudes. Seasonal vari- and adjust their development independent of maternal ation in offspring phenotype often reflects phenotypic plas- effects in eggs. ticity [e.g. older, more experienced adults nesting early and Patterns of embryonic growth are altered when there is producing higher quality chicks than later nesting, inexperi- a mismatch between maternal cues of season and photope- enced adults (Daunt et al. 2007; Nisbet & Dann 2009)]. riod cues of season. For example short day lengths appear Variation in body size among populations that vary across to mitigate seasonal egg effects; when late season eggs are latitudes has been interpreted as evolutionary adaptation; exposed to short days during development, tarsi lengths however, recent studies suggest that phenotypic plasticity is are similar to that of hatchlings from early season eggs a mechanism contributing to latitudinal variation in pheno- (Fig. 2). In this case, embryos in late season eggs appear types (Gienapp et al. 2008; Husby, Hille & Visser 2011). to be sensing photoperiod directly and altering their phe- The influence of photoperiod on offspring development and notype. The main effects of season and photoperiod on growth provides a mechanism by which phenotypic plastic- yolk sac reserves are driven by the early season eggs ity might be generated along both seasonal and latitudinal exposed to mismatched day lengths having more yolk sac gradients, especially for species breeding across a wide reserves than hatchlings in all other treatments (Fig. 3). range of latitudes (such as Franklin’s gull). The amount of yolk in eggs prior to incubation does not In order for embryos to respond to a cue of season, they change seasonally, suggesting that the amount of energy must possess the appropriate sensory capacity (Reed & used during development is reduced for early season eggs Clark 2011). In birds, the central sensory system that exposed to long day lengths. This is likely because of detects and organizes the response to day length involves

© 2012 The Authors. Functional Ecology © 2012 British Ecological Society, Functional Ecology, 26, 948–958 956 M. E. Clark & W. L. Reed cells in the retina, pineal gland and the suprachiasmic site and logistical support, and we especially thank C, Dixon, G. Erickson, nuclei in the hypothalamus (Dawson et al. 2001). The eye S. Fellows, T. Grant, T. Gutzke and B. Vose for their cooperation. Fund- ing was provided by the National Science Foundation (IOS-0445848 to W. is one of the first sensory organs to develop (Hamburger & L.R. and M.E.C.), North Dakota Game & Fish Department (to M.E.C. Hamilton 1951), and in birds, the retina can produce mela- and W.L.R.) and the U.S. Fish & Wildlife Service (M.E.C.). Fieldwork was tonin, a hormone produced in the absence of light that conducted under permits from North Dakota Game & Fish Department, U.S. Fish & Wildlife Service and North Dakota State University Institu- affects growth and immune function (Dawson et al. 2001; tional Animal Care and Use Committee. Paulose et al. 2009). In the case of Franklin’s gull and other free-living populations (Cooper et al. 2011), we do not know the specific mechanism responsible for embry- References onic responses to photoperiod. However, consistent with Ackerman, J.T. & Eagles-Smith, C.A. (2010) Accuracy of egg flotation our experimental evidence in the gull, agricultural throughout incubation to determine embryo age and incubation day in researchers have shown that poultry embryos also respond waterbird nests. Condor, 112, 438–446. Archer, G.S., Shivaprasad, H.L. & Mench, J.A. (2009) Effect of providing to the length of light exposure during incubation (Siegel light during incubation on the health, productivy and behavior of broiler et al. 1969a; Shafey 2004b) and have identified that chickens. Poultry Science, 88,29–37. chicken embryos produce melatonin early in development Beldade, P., Mateus, A.R.A. & Keller, R.A. (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Molecular Ecology, (Paulose et al. 2009). Furthermore, when chicken embryos 20, 1347–1363. are exposed to increasing levels of light during incubation, Benowitz-Fredericks, Z.M. & Kitaysky, A.S. (2005) Benefits and costs of they increase rates of feeding and growth after hatching rapid growth in common murre chicks Uria aalge. Journal of Avian Biol- ogy, 36, 287–294. (Archer, Shivaprasad & Mench 2009). Our hypothesis for Berg, E.A. (2009) Effects of nest site environment and timing of breeding on the adaptive significance for an embryo in the wild that reproductive success in Franklin’s gulls (Larus pipixcan). M.S., North hatches late in the season, when day lengths are longer, is Dakota State University. Biard, C., Gil, D., Karadas, F., Saino, N., Spottiswoode, C.N., Surai, P.F. a change in growth, which allows them to leave the nest at & Moller, A.P. (2009) Maternal effects mediated by antioxidants and the an earlier age and prepare for migration in a shorter evolution of Carotenoid-based signals in birds. American Naturalist, 174, period of time. 696–708. Boonstra, T.A., Clark, M.E. & Reed, W.L. (2009) Maternal resource varia- The findings from this study enhance our understanding tion across the laying sequence in Canada geese Branta canadensis max- of the ecological and evolutionary context of shifts in sea- ima. Journal of Avian Biology, 40, 520–528. sonal timing of breeding events. Temperature affects nest Bozenna, O., Pawel, M., Bogdan, L. & Urszula, S. (2007) Melatonin and its synthesizing enzymes (arylalkylamine N-acetyltransferase-like and initiation in birds (Visser, Holleman & Caro 2009), and hydroxyindole-O-methyltransferase) in avian eggs and early embryos. temperate species are observed to initiate breeding earlier Journal of Pineal Research, 42, 310–316. in conjunction with global changes in climate (Winkel & Bradshaw, W.E. & Holzapfel, C.M. (2007) Evolution of animal photoperiodism. Annual Review of Ecology, Evolution and Systematics, 38, Hudde 1997; Dunn 2004; Potti 2009). Research on season- 1–25. ality in avian reproduction must consider the direct impact Bradshaw, W.E. & Holzapfel, C.M. (2008) Genetic response to rapid cli- of photoperiod on embryonic development and not only mate change: it’s seasonal timing that matters. Molecular Ecology, 17, 157–166. the effects of date mediated through parental care or pro- Bradshaw, W.E. & Holzapfel, C.M. (2010) Light, time, and the physiology visioning. Our results, in conjunction with those of Cooper of biotic response to rapid climate change in animals. Annual Review of et al. (2011), suggest that differences in photoperiod result- Physiology, 72, 147–166. Burger, J. & Gochfeld, M. (1994) Franklin’s gull: Larus pipixcan. Birds of ing from earlier nesting or from shifts in habitat across lat- North America (eds A. Poole & F. Gill), pp. ???–???. American Ornithol- itudes can alter avian embryonic development and size at ogists’ Union & Academy of Natural Sciences, Washington, DC and hatching, which is an unexplored consequence of climate Philadelphia, PA. Cooper, C.B., Voss, M.A., Ardia, D.R., Austin, S.H. & Robinson, W.D. change. Little is known about the impacts of maternal (2011) Light increases the rate of embryonic development: implications effects under climate change. However, our knowledge of for latitudinal trends in incubation period. Functional Ecology, 25, 769– the fitness consequences of maternal effects present after 776. Coppack, T., Pulido, F. & Berthold, P. (2001) Photoperiodic response to hatching suggests the impacts to be maladaptive (Coppack, early hatching in a migratory bird species. Oecologia, 128, 181–186. Pulido & Berthold 2001; Visser 2008). If the timing of nest- Daunt, F., Wanless, S., Harris, M.P., Money, L. & Monaghan, P. (2007) ing shifts outside of the range experienced in the species’ Older and wiser: improvements in breeding success are linked to better foraging performance in European shags. Functional Ecology, 21, 561– evolutionary history in response to environmental changes 567. (e.g. warming spring temperatures), the interaction Dawson, A., King, V.M., Bentley, G.E. & Ball, G.F. (2001) Photoperiodic between maternal and photoperiodic effects on offspring control of seasonality in birds. Journal of Biological Rhythms, 16, 365– 380. development may compromise resilience to change. Dmitriew, C.M. (2011) The evolution of growth trajectories: what limits growth rate? Biological Reviews, 86,97–116. Drent, R.H. (2006) The timing of birds’ breeding seasons: the Perrins Acknowledgements hypothesis revisited especially for migrants. Ardea, 94, 305–322. Dunn, P. (2004) Breeding dates and reproductive performance. Birds and We thank B. Clark, J. Froehlich, D, Larsen, P. Martin, J. Peterson, Climate Change (eds A.P. Moller, W. Fielder & P. Berthold), pp. 69–87. S. Weissenfluh and E. Berg for assistance in the field and laboratory. Early Academic Press Ltd, London. drafts of the manuscript were generously reviewed by B. Lyon, J. Bowsher French, S.S., Greives, T.J., Zysling, D.A., Chester, E.M. & Demas, G.E. and the Gillam, Clark, Reed Lab group. Three anonymous reviewers and (2009) Leptin increases maternal investment. 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