Study Site and Species

We conducted our study at the Common Tern colony site “Banter See” in Wilhelmshaven, Germany (53°30′40′′N, 08°06′19′′E), where birds breed on 6 rectangular concrete islands surrounded by a 60-cm high wall. Since 1984, all fledglings have been banded, and, since 1992, additionally fitted with TROVAN ID-100 subcutaneous transponders (Trovan, UK; for details, see Becker and Wendeln 1997). These transponders allow lifelong identification of terns through the use of resting platforms within the colony, where antennas remotely and automatically record and save the individual alphanumeric codes of all birds on the platforms every 5 sec, together with the time of day. Due to the marking program, all birds bred at the colony are of known age. The sex of all birds has also been determined by molecular methods (since 1998) or observation (until 1997). Each breeding season, breeding pairs are identified by putting an antenna around each nest for 1–2 days (usually during midincubation; Becker and Wendeln 1997). The colony is checked 3 times weekly, and new nests are marked, eggs are measured and labeled according to laying order, and newly hatched chicks are banded. At every check, the individual ID and weight of each chick is recorded until fledging (usually within 27 days; Becker and Wink 2003).

Data Collection

Our study was conducted in 4 yr (2008, 2009, 2010, and 2012), in which the number of breeding pairs ranged from 355 to 410 and annual reproductive success averaged 0.33–1.20 chicks per pair. We sampled a total of 41 pairs (2008: n = 10, 2009: n = 15, 2010: n = 11, 2012: n = 5) for which both mates were of known age and history. We recorded nest attendance during incubation and chick rearing for 29 pairs, and during chick rearing only for 12 pairs. ‘Day' was defined as the duration from sunrise to sunset, and ‘night' as the time from sunset to sunrise, using exact data for Wilhelmshaven ( www.sunrise-and-sunset.com). Nest attendance of both pair mates was recorded by plate antennas (model AAN FK2, AEG Identifikationssysteme, Ulm, Germany; reading distance up to 24 cm), which were put underneath the nest for several days (average = 9 ± 3 SD days). Around 6 recordings of a bird per min were obtained and used to determine the start and end of each incubation shift. With these values, we built the mean proportion of daytime and nighttime recordings for males and females, time with no parent bird at the nest, and time when the system was shut down for each 24-hr interval. Afterward, periods when the system was shut down were excluded, and a mean value for day and night was calculated for each breeding phase (incubation vs. chick rearing; Table 1).

TABLE 1.

Recorded nest attendance (%), sex-specific nest attendance (SNA), and total nest attendance (TNA) during the day and at night during incubation and chick rearing for male and female Common Terns, and time periods when no bird was recorded and when the system was shut down, in northern Germany.

We analyzed 2 types of nest attendance: (1) Sex-specific nest attendance (SNA), defined as the proportion of time that the male or female was recorded at the nest (Table 1). In this case, time periods when no parent was recorded at the nest were not taken into account. This measure was used to compare nest attendance between the sexes and related to factors such as breeding experience, time of day, and breeding phase; and (2) Total nest attendance (TNA), defined as the proportion of time when at least one member of a pair was registered as present at the nest, also taking into account periods when no parent bird was incubating or brooding (Table 1). In this case, nest attendance was recorded per pair as a measure of parental behavior in relation to breeding success or experience.

Birds may occasionally be quite motionless when incubating, in which case they may not be recorded by the system for several minutes (18–28%; ‘no one' in Table 1). To clarify whether birds were still incubating during these periods, we used another set of data collected by scales installed underneath the nest (Riechert et al. 2014b; Appendix). These scales recorded body mass in addition to ID of birds, as well as time of day. Using these data, we found that the presence of breeders was less well recorded (longer gaps between recordings) by the antennas at night than during the day (body mass was recorded by the scales all the time; Appendix Table 6). Furthermore, body weight data showed that terns had significantly shorter periods of absence from the nest during the night than during the day (Wilcoxon test: Z = −3.82, P = 0.02, n = 12), and that a change between mates was reliably recorded by antennas as birds move when they replace each other at the nest during incubation and chick guarding. Moreover, changes between pair mates, as well as the presence or absence of a breeder recorded by the system, showed a high correlation (95%) with behavioral observations (A. Vulcano personal communication). For these reasons, we assumed parents to be incubating the entire night (Table 1), even if gaps in recordings were noticed. In contrast, during the day, terns are known to sometimes leave the clutch unattended for several minutes to defecate, drink, feed, or just rest nearby (Becker and Frank 1990). If these gaps were longer than 10 min, they were treated as time with no parent present (Table 1), which may potentially have led to an underestimation of incubation consistency for Common Terns. For all analyses, we used the corrected calculated attendance data from total recordings for males and females (values in parentheses in Table 1). However, for all these analyses, we note that we did not use behavioral observations, but used antenna recordings to analyze nest attendance.

Antennas were put under the nest 4 ± 2 (mean ± SD) days before the first chick hatched and were left there until 7 ± 2 days after the first chick hatched. All birds accepted this interference at their nests and continued their breeding activities. As Common Tern chicks start to move away from the nest ∼3–4 days after hatching, when parents also start to leave them unattended (Wiggins 1989, Becker and Ludwigs 2004), and are not recorded reliably all day, we restricted our dataset up to the day when the youngest chick was 2 days old. For analyses of SNA, we calculated the mean nest attendance during each phase (incubation and chick rearing) for each sex during the day and night. Likewise, for TNA, the mean value for each phase was calculated per pair.

For each pair, relative hatching and chick rearing success were calculated by subtracting the individual pair's values from the annual colony means of hatching and rearing success, respectively. For rearing success, we used the number of chicks that were alive at day 10 to be able to best relate this metric to nest attendance during the first days of life (until the youngest chick was 2 days old).

Blood Sampling

Blood samples were taken from 39 birds (both members of 17 pairs, plus 5 single pair mates) to analyze hormone levels: (1) From 5 pairs and 4 single pair members, we took a sample only during midincubation (9–15 days after clutch completion); (2) from 2 pairs, we took a sample only during chick rearing (1–5 days after hatching of the first chick); and (3) from 7 pairs and 4 singe pair members, we took samples during both breeding phases. For a subset of 27 of these 39 birds (15 males and 12 females), we were able to measure nest attendance and hormone levels on the same day (for 2 pairs plus 1 single pair member during incubation, 6 pairs plus 4 single pair members during chick rearing, and 3 pairs during both phases).

Blood samples were taken minimally invasively by using blood-sucking bugs (Dipetalogaster maxima) in hollow eggs (Becker et al. 2006). Sampling took place in the early morning, between 0500 and 0900 hours, to minimize diurnal variation in hormone levels. Hungry bugs were placed in hollow eggs and, after the target bird was identified as being on the nest by the antenna, the whole clutch was replaced with dummy eggs including the egg containing the bug. Birds resumed incubating immediately. After bugs had finished their meals, ∼20–30 min later, the dummy eggs were retrieved and tern eggs replaced in the nest. Blood was then extracted from the bugs into a syringe. This method has been successfully validated for baseline prolactin (Riechert et al. 2012) and corticosterone (Arnold et al. 2008) and worked well (average success of bugs taking enough blood: 87%; range: 80–97%). Samples were put on ice immediately, and were centrifuged and stored at −20°C within 4–5 hr of collection.

Hormone Analyses

Baseline concentrations of hormones were analyzed at the Centre d'Etudes Biologiques de Chizé, France, by radioimmunoassay (RIA). Following Cherel et al. (1994), prolactin levels were determined twice for each sample after validation for our species and study site (Riechert et al. 2012). Prolactin levels showed a dose-dependent, parallel response curve to the prolactin of chicken plasma (chicken plasma was sourced from the UCLA Medical Center, Los Angeles, California, USA). Total baseline corticosterone level was determined from the remaining plasma (25 μL) after ethyl ether extraction following the methods of Lormée et al. (2003). The lowest corticosterone measurement was 0.42 ng mL⁻¹, while the minimum detection level was 0.10 ng mL⁻¹. Due to a large overall sample size in most years, samples were run in different assays (2008: n = 4, 2009: n = 4, 2010: n = 3, 2012: n = 2). However, assay identity had no effect on baseline corticosterone level (Riechert et al. 2012), and the coefficient of variation for intra- and inter-assay variation was within a range of 6–11% (n = 4 duplicates of reference sample for intra-assay variation).

Statistics

Sex-specific Nest Attendance

Females showed higher nest attendance than males, during both incubation and chick rearing, and during the day and at night (t-test: incubation, daytime: t = −3.31, P = 0.003, n = 58; chick rearing, daytime: t = −7.58, P < 0.001, n = 82; Wilcoxon test: incubation, nighttime: z = −2.95, P = 0.003, n = 58; chick rearing, nighttime: z = −4.94, P < 0.001, n = 82; Figure 1). Breeding experience of females, but not males, showed a tendency to be correlated with mean nest attendance calculated over the whole breeding period (r = 0.28, P = 0.07, n = 41, and r = 0.16, P = 0.32, n = 41, respectively).

FIGURE 1.

Average (± SE) nest attendance (proportion of time) of male (filled circles) and female (open circles) Common Terns during incubation and chick rearing during the day and at night, in northern Germany. Asterisks above error bars indicate significant differences between the sexes (** P < 0.01, *** P < 0.001), whereas letters mark differences within the sexes. Sample sizes (n) for pairs are presented at the bottom of the graph.

Our model selection procedure indicated that variation in nest attendance (SNA) in males was best explained by breeding phase, time of day, and the interaction between time of day and experience (Table 2). Mean male nest attendance was significantly lower during chick rearing at nighttime than during all other phases and times (rearing, daytime: z = −2.88, P = 0.004, n = 41 males; incubation, daytime: z = −3.99, P < 0.001, n = 29; incubation, nighttime: z = −2.65, P = 0.008, n = 29; Figure 1). Moreover, male nest attendance during incubation was significantly higher during the day than at night (z = −2.26, P = 0.02, n = 29) as well as during the day when rearing chicks (t = −2.59, P = 0.02, n = 29). SNA during the day was not related to breeding experience of males (r = 0.02, P = 0.89, n = 41); at night, however, there was a slight tendency for more experienced males to attend the nest for a greater proportion of time than less experienced males (r = 0.37, P = 0.15, n = 41), though this difference was far from significant. Hormone values measured during both breeding phases were not found to be significantly correlated with mean SNA in males (Table 2).

TABLE 2.

Results of a linear mixed effects model analyzing nest attendance by male Common Terns in northern Germany in relation to breeding phase, time of day, breeding experience, and hormones, as well as the interactions between these terms. The best model (after stepwise backward elimination of parameters) is shown on the left-hand side, and parameter values at extraction on the right-hand side. For the variable Year, Wald Z = 0.84, P = 0.38; and for Bird ID, Wald Z = 3.07, P = 0.04.

For females, the best model contained time of day, breeding phase, and the interaction of breeding experience with breeding phase (Table 3). Female nest attendance differed between breeding phases (χ²_3,29 = 23.07, P < 0.001), with significantly higher attendance during chick rearing at night than during all other phases and times (incubation, day: z = −3.73, P < 0.001, n = 29 females; incubation, night: z = −2.39, P = 0.02, n = 29; rearing, day: z = −2.72, P = 0.007, n = 41; Figure 1). Moreover, daily nest attendance was significantly lower during daytime incubation than daytime chick rearing (t = −2.63, P = 0.01, n = 29) as well as nighttime incubation (z = −2.26, P = 0.02, n = 29).

TABLE 3.

Results of a linear mixed effects model analyzing nest attendance by female Common Terns in northern Germany in relation to breeding phase, time of day, breeding experience, and hormones, as well as their interactions. The best model (after stepwise backward elimination of parameters) is shown on the left-hand side, and parameter values at extraction on the right-hand side. For the variable Year, Wald Z = 0.68, P = 0.50; and for Bird ID, Wald Z = 2.47, P = 0.04.

During incubation, there was a tendency for more experienced females to exhibit higher nest attendance than less experienced ones (r = 0.42, P = 0.09, n = 41), whereas no relationship was found during chick rearing (r = 0.12, P = 0.27, n = 41). As with males, prolactin and corticosterone values measured in females did not show a significant correlation with SNA during incubation and brooding (Table 3). For both sexes, year of sampling did not contribute significantly to variation in SNA (Tables 2 and 3); however, individual identity explained a significant part of the remaining variance in attendance data (Tables 2 and 3), indicating large interindividual variation in nest attendance.

Total Nest Attendance and Breeding Success

Variation in the relative hatching and chick rearing success of pairs was explained by breeding phase, mean experience of pairs, and the interaction between breeding phase and TNA (Table 4). TNA during incubation was quite variable (mean: 0.86 ± 0.10, range: 0.58–0.98), but was not related to hatching success (r_s = 0.14, P = 0.44, n = 29) or incubation duration (r_s = −0.10, P = 0.59, n = 29). During chick rearing, TNA differed between pairs (mean: 0.78 ± 0.12, range: 0.46–0.95), and parents with higher nest attendance during early brood rearing raised significantly more chicks (r_s = 0.35, P = 0.03, n = 41; Figure 2).

TABLE 4.

Results of a linear mixed effect model analyzing pair breeding success of Common Terns in northern Germany in relation to breeding phase, total nest attendance (TNA), and breeding experience, as well as the interactions between these terms. The best model (after stepwise backward elimination of parameters) is shown on the left-hand side, and parameter values at extraction on the right-hand side. For the variable Year, Wald Z = 1.90, P = 0.13; and for Nest ID, Wald Z = 2.51, P = 0.07.

FIGURE 2.

Nest attendance per Common Tern pair (proportion of time with one parent present) during chick rearing in relation to the relative number of fledglings (colony mean minus individual data) in northern Germany.

Pairs with greater mean breeding experience raised more chicks during early chick rearing than less experienced pairs (r_s = 0.53, P = 0.001, n = 41). For pairs that were sampled during both breeding phases, relative hatching success was significantly higher than relative early chick rearing success (0.13 vs. −0.15, Z = −3.63, P = 0.002, n = 29). Furthermore, parents with high attendance during incubation also showed a tendency to exhibit higher attendance during brood rearing (r_s = 0.33, P = 0.07, n = 29). Nest ID was marginally significant, illustrating differences in success between pairs (Table 4).

Attendance Patterns and Hormone Levels

Using a subset of data with synchronous measurements of hormones and nest attendance within 1 day (to account for seasonal variation in hormone levels), we found no significant correlation between prolactin or corticosterone level and nest attendance during incubation or chick rearing for either sex (incubation: males, r < 0.5, P > 0.3, n = 5; females, −0.3 < r < 0.0, P > 0.6, n = 6; rearing: males, −0.3 < r < 0.0, P > 0.4, n = 13; females, −0.1 < r < 0.0, P > 0.9, n = 9). However, taking into account time of day and breeding phase, a pattern was revealed: In the chick rearing phase, during the day, males with elevated prolactin levels exhibited slightly higher nest attendance (r = 0.51, P = 0.07, n = 13; Figure 3A). In addition, males with elevated baseline levels of corticosterone tended to show lower daytime nest attendance (r = −0.51, P = 0.08, n = 13; Figure 3B). However, for males during incubation and for females during both breeding phases, we did not find a significant correlation of either hormone with nest attendance (−0.5 < r < 0.5, P > 0.1, 4 < n < 10).

FIGURE 3.

(A) Baseline prolactin (ng mL⁻¹) and (B) baseline corticosterone (ng mL⁻¹) of male Common Terns in relation to nest attendance during daytime chick rearing, in northern Germany.

Corticosterone values did not change between the breeding phases in either sex, and nor did prolactin values in females (Table 5). Males, on the other hand, exhibited significantly lower prolactin values during chick rearing compared with incubation (Table 5).

TABLE 5.

Hormone concentrations (ng mL^–1; PRL = prolactin, CORT = corticosterone) per breeding phase and pair mate of Common Terns in northern Germany. A t-test for related samples was used; significant P-values are highlighted in bold font.

Prolactin values during both phases, as well as corticosterone values during incubation, were not significantly correlated between pair members (r < 0.5, P > 0.3, n = 7). During rearing of chicks, however, a trend toward a negative correlation between corticosterone values of pair members was found (r = −0.72, P = 0.07, n = 7). Regarding the change in hormones between the 2 breeding phases, values for pair members were not significantly related to each other (r < 0.3, P > 0.5, n = 7).

In females, but not males, greater breeding experience was positively correlated with a change in prolactin values from incubation to chick rearing (females: r = 0.78, P = 0.04, n = 7; males: r = −0.26, P = 0.50, n = 11). Similarly, in the case of corticosterone, greater experience in females, but not males, was marginally significant and slightly positively correlated with an increase from incubation to chick rearing (females: r = 0.68, P = 0.09, n = 7; males: r = −0.21, P = 0.55, n = 11). We did not find any correlation between prolactin or corticosterone and hatching or rearing success in males or females (−0.4 < r_s < 0.3, P > 0.3 in every case, n = 11 and 7 for males and females, respectively).

Sex- and Phase-dependent Daytime and Nighttime Nest Attendance

Consistent with the findings of previous studies (Wiggins and Morris 1987, van der Winden 2005), our results clearly confirm sex-specific parental care in Common Terns: Females spent a greater proportion of time incubating eggs and brooding small chicks than their mates. This pattern was especially pronounced at night (see also Nisbet 2002), as has also been found in Western Gulls (Larus occidentalis; Pierotti 1981). This pattern is not universal, however, and can be reversed, as is found in Black Terns (Chlidonias niger; van der Winden 2005), Thick-billed Murres (Uria lomvia; Jones et al. 2002), and various sandpipers (Byrkjedal 1985, Bergstrom 1986, Warnock and Oring 1996). However, we assume that male Common Terns often rest near the nest while the female is incubating (see also Wiggins and Morris 1987, Weidinger 1998, Nisbet 2002). But is the pattern of female-biased Common Tern nest attendance a general one, or might sex-specific parental attendance change under certain conditions? Common Terns are not able to defend their eggs or chicks against nocturnal predators (Wendeln and Becker 1999b, Nisbet 2002), and it would be particularly interesting to analyze parental attendance under the pressure of nocturnal predation.

Comparable with the results of prior studies of Common Terns (Wiggins and Morris 1987, Burness et al. 1994, Galbraith et al. 1999) and Black Terns (van der Winden 2005), and in line with our prediction, males were rarely detected on the nest after young hatched. During the first week of chick rearing, the female mostly stayed with the chicks, while the male predominantly foraged and fed the young (Wiggins and Morris 1987, Wendeln 1997). Accordingly, the feeding rate, which is normally ∼1 food item per chick per hour in this colony (Frank 1992), was found to be much higher in males than in females (Wendeln 1997). The lower nest attendance of males during incubation may allow them more time to find and exploit suitable foraging grounds (Becker et al. 1993, Wendeln 1997), in order to be prepared and save time and energy once the chicks hatch and have to be fed regularly and frequently with larval fish.

In line with our expectation, the breeding experience of Common Terns did affect nest attendance. Older females spent more time at the nest during incubation than younger ones, and more experienced males exhibited increased nest attendance at night. It is known that Common Terns need several years to become proficient at foraging and chick provisioning (Limmer and Becker 2009, 2010), and therefore more experienced birds are able to spend more time at the nest. However, as mentioned previously, we assume that males stay close to the nest even when they are not incubating or brooding. Females might have a stronger drive to incubate than males, possibly leading to the fact that experienced females increase nest attendance during incubation, while males rest near the nest after foraging.

Year did not have a significant effect on nest attendance, illustrating that, on average, Common Terns maintain constant breeding behavior under different conditions. Other factors, such as experience and quality of the pair, have a much greater effect on breeding behavior.

Reproductive Success and Nest Attendance

Low parental attentiveness to the clutch can prolong the incubation period and increase the risk of predation (Aldrich and Raveling 1983, Pienkowski 1984). Parental attendance at the nest was quite variable between Common Tern pairs; however, interpair variability was not related to hatching success or incubation duration. Though linked to parental quality (Wendeln and Becker 1999a), hatching success in the Banter See colony was relatively high overall during the years of this study (Riechert et al. 2014a). This could be one reason for no link being found with nest attendance. Another reason could be the fact that eggs hatch even after being left unattended for periods of time (Sudmann et al. 1994, Stoleson and Beissinger 1999), supported by the finding that embryos of Common Terns and many waders are quite robust to fluctuations in temperature (Myhre and Steen 1979). Egg predation of unattended clutches during the day is rare in the Banter See colony (Becker 1998). Only complete nights without incubation due to nocturnal predator activity led to prolonged incubation and decreased hatching success (Sudmann et al. 1994, Wendeln and Becker 1999b).

In line with our prediction, parental nest attendance during chick rearing was positively correlated with rearing success up to day 10, which was much more variable than hatching success. Our recording of nest attendance was restricted to only the first days of the rearing period, until the smallest chick was 2 days old. This is the period when the semiprecocial chicks need to be brooded by the parents (Nisbet 2002, Becker and Ludwigs 2004). There are many more factors that affect fledging success, such as feeding rate and food quality (Massias and Becker 1990, Quillfeldt 2001). However, high nest attendance during the first few days may reflect high individual quality, contributing to early chick survival in various ways and thereby enhancing breeding success. Similarly, chick survival in the Antarctic Petrel (Thalassoica antarctica) was high after constant guarding by parents, even beyond thermoregulatory needs (Varpe et al. 2004). Furthermore, chicks of the Snow Petrel (Pagodroma nivea) that were left alone at day 4 exhibited lower growth rates and survival than chicks that were abandoned at an older age, reflecting low parental quality (Amundsen 1995). Besides exposure to hunger, rain, or cold, Common Tern chicks at Banter See that are left alone can be attacked by neighbors in this dense breeding colony, and sometimes die due to their injuries (J. Riechert and P. Becker personal observations).

Breeding success did not differ significantly between years in this study. Other studies of seabirds have found clear effects of year on reproductive success (e.g., Becker 1998, Quilllfeldt 2001, Golet et al. 2004) and, in a previous study, we also showed that reproductive success was significantly different between years in this Common Tern colony (Riechert et al. 2014a). However, sample sizes were much higher in these studies.

Influence of Hormone Levels on Nest Attendance

Because hormone levels exhibit diurnal variation (Lea et al. 1982, Romero and Remage-Healey 2000) and were only measured during the day, we restricted our analyses to daytime nest attendance patterns. Prolactin levels have been suggested to be directly linked to the amount of parental care (reviewed by Angelier and Chastel 2009), and sex-specific parental care has been shown to be reflected in prolactin values: The sex that contributed more to incubation or rearing of young exhibited higher prolactin levels during the respective breeding phase (Lormée et al. 2000, Schmid et al. 2011). In line with our prediction, we found that prolactin values after hatching were reduced in males, but not in females, and that males with reduced prolactin values exhibited lower nest attendance. Likewise, male and female Black-legged Kittiwakes (Rissa tridactyla), which spend much time at sea resulting in reduced nest attendance, exhibit low prolactin values (Angelier et al. 2009).

High parental effort could lead to reduced body reserves, reflected in low prolactin values, as shown in kittiwakes and Adelie Penguins (Pygoscelis adeliae), ultimately lowering nest attendance (Angelier et al. 2009, Spée et al. 2010). Consistent with this finding, from a prior study we know that Common Terns with a considerable loss in body mass due to a long incubation bout are characterized by decreased prolactin values compared with their satiated state (Riechert et al. 2014b). The current study has linked this result with nest attendance, demonstrating that lower prolactin values are accompanied by reduced nest attendance. Due to high foraging effort, males might lose more weight than females, and their contact with chicks is lower, which is reflected in lower prolactin values after hatching.

Parents with low nest attendance during chick rearing were characterized not only by low prolactin, but also by increased baseline corticosterone, matching our prediction. This is the next step and logical consequence of the preceding study (Riechert et al. 2014b), which demonstrated low prolactin and increased corticosterone in birds with low body condition. Experimentally increased corticosterone levels resulted in lower nest attendance of kittiwakes as well (Kitaysky et al. 2001, Angelier et al. 2009). Moderately elevated corticosterone is known to trigger activity (Astheimer et al. 1992, Angelier et al. 2007), and increase foraging effort (Kitaysky et al. 2001, Crossin et al. 2012) and feeding of young (Koch et al. 2002, Doody et al. 2008, Bonier et al. 2009). Common Terns caring for chicks show high parental effort (Wendeln and Becker 1999b), which has been linked with elevated baseline corticosterone values in several species (Harding et al. 2009, Miller et al. 2009, Bonier et al. 2011). On the other hand, elevated corticosterone achieved by implantation and reaching the stress level is known to negatively affect reproduction (reviewed by Angelier and Chastel 2009). Common Terns were characterized by lower body mass and increased corticosterone levels at the end of an incubation bout compared with the start of the incubation bout (Riechert et al. 2014b). In line with this, in Dovekies (Alle alle), experimental evidence has been found that increasing mass loss results in elevated baseline corticosterone values in both sexes (Harding et al. 2009). As Common Terns lose much more body mass during chick rearing than incubation (Wendeln and Becker 1996, Wendeln 1997), their increased corticosterone levels could indicate low reserves and may stimulate foraging and food intake.

Hormone values were not significantly correlated between pair members, except those of corticosterone during chick rearing, which showed a negative correlation. This could indicate that higher foraging activity in males, reflected in enhanced corticosterone values, might lead to lower activity in females, as males might provision the young sufficiently.

While rearing chicks, experienced females exhibited increased prolactin and corticosterone values compared with younger females. From previous studies in this colony, we know that greater experience can be linked with increased foraging success and body weight (Limmer and Becker 2007, 2009). Riechert et al. (2014b) indicated that the change in hormones is more pronounced under stronger energy constraints during chick rearing compared with incubation, which is also illustrated by the present study that additionally integrated data on breeding behavior to complete the picture.

During chick rearing, we found a much stronger relationship between hormone levels and nest attendance in males compared with females. This is in line with the results of Wiggins and Morris (1987), Burness et al. (1994), and Wendeln (1997), who all showed higher feeding effort by male Common Terns, especially during the first week of rearing. On the other hand, females were more constrained in their own feeding than males, as they were engaged in breeding activities most of the time, reflected in their high mass loss during rearing of chicks (Wendeln and Becker 1996, Wendeln 1997). Parental maintenance is further hampered by the marine environment of the Wadden Sea, where foraging success depends on the tidal cycle (Frank and Becker 1992). Higher male activity and foraging effort in line with the new role as feeder after hatching of chicks is reflected in reduced nest attendance, lower baseline prolactin levels, and increased corticosterone values. In this respect, the current study integrates measures of behavior and hormonal data into the already existing data on body condition, breeding experience, reproductive success, and hormone values, thereby completing the picture of the regulation of breeding in Common Terns.

Conclusions

We integrated measures of nest attendance, reproductive success, and hormonal status during incubation and chick rearing in Common Terns, enabling a more detailed insight into the regulation of avian breeding behavior. Different parental roles were indicated by sex-specific temporal patterns based on interactions between hormones and nest attendance during incubation and rearing, modified by the breeding experience of the parents. Further studies should address whether sex-specific nest attendance and vulnerability may change under adverse environmental conditions, such as the presence of nocturnal predators. Investigations during the later stages of chick rearing should clarify if females, like males, exhibit changes in hormone levels when they start extensively feeding chicks as well. Furthermore, it would be interesting to analyze intraindividual plasticity in behavior by comparing parental care, hormones, and reproductive success from favorable and unfavorable breeding seasons.