Ornis Fennica 86:140–148. 2009

Sex-specific parental care by incubating Little (Alle alle)

Katarzyna Wojczulanis-Jakubas, Dariusz Jakubas & Lech Stempniewicz

K. Wojczulanis-Jakubas, University of Gdañsk, Department of Vertebrate Ecology and Zoology, al. Legionów 9, 80-441 Gdañsk, Poland. E-mail [email protected] (corres- ponding author) D. Jakubas, University of Gdañsk, Department of Vertebrate Ecology and Zoology, al. Legionów 9, 80-441 Gdañsk, Poland. E-mail [email protected] L. Stempniewicz, University of Gdañsk, Department of Vertebrate Ecology and Zoology, al. Legionów 9, 80-441 Gdañsk, Poland. E-mail [email protected]

Received 24 March 2009, accepted 11 August 2009

The evolution ofsex-specific reproductive behavior among species with biparental care promotes sexual conflict over care. Such conflict may be less intense in species with long- term pair bonds. We examined sex-specific patterns of care during the incubation period in a monogamous, colonially breeding seabird ofthe high region, the Little (Alle alle). We recorded time spent by ofknown sex in- and outside the nest, and the frequency ofparticular activities (aggressive interactions and collection ofnest material), during four continuous 24-h watches. Males and females shared the incubation duty equally. Both sexes participated in the off-incubation duty behavior with similar fre- quency. However, males attended nest-site territories more than females and were thus more often involved in aggressive interactions and nest-material collection. These results suggest that there were sex-specific patterns of engagement in different forms of parental care during the incubation period.

1. Introduction favors their future breeding success (Mock & Fuijoka 1990, Flower 1995). For many species, biparental care is crucial Although both parents have to cooperate dur- for successful breeding (Lack 1968, Gowaty 1996, ing reproduction, sex-specific patterns of parental Sydeman et al. 1996). The participation ofboth care are commonly found. Such sex-specific pat- partners in brood care allows each ofthem to save terns ofparental care reflecta variety ofmale and energy, thereby enabling them to increase their female constraints imposed by physiological, be- own fitness. Particularly, in species with long-ter- havioral and environmental factors, with members m monogamy, such as many seabirds (e.g., del ofeach sex aiming to maximize their own lifetime Hoyo et al. 1996, Gaston & Jones 1998), individu- reproductive success (Trivers 1972). Conse- als are less likely to exploit their partners because quently, understanding sex-specific patterns of pa- maintaining the condition oftheir partner en - rental care is important to comprehend the evolu- hances the fitness ofboth members ofthe pair and tion ofparental strategies. Wojczulanis-Jakubas et al.: Parental care by incubating Little Auks 141

Most studies dealing with sex differences in od, whereas it increased (lower H/L ratio) in parental care have been focused on the chick-rear- males. This difference may indicate sex-specific ing period. While that period has traditionally been differences in parental behavior during incuba- regarded as the most demanding period ofavian tion. reproduction (e.g., Drent & Daan 1980), incuba- To compare sex-specific parental care of incu- tion has been evidenced to be an important compo- bating Little Auks we considered not only the in- nent ofthe reproductive cost, and birds expend a cubation duties but also time spent and behavior considerable amount ofenergy both during egg in - performed during the birds’ attendance in their ter- cubation in the nest and also during doing parental ritory, but outside the nest chamber. Seven types duties outside the nest, including nest-site defense ofbehavior, performed by birds during territory and maintenance (e.g., Monaghan & Nager 1997, attendance, were as follows: laying down/sitting, Thomson et al. 1998, Reid et al. 2002, Tinbergen walking, preening, sleeping, head-wagging (head & Williams 2002). The behavior ofparents during movements from side to side, performed in pairs, incubation may reflect their earlier investments with unknown behavioral meaning; Evans 1981), and affect their behavior in later stages ofthe aggressive interactions and collection ofnest ma - breeding cycle, and also their future reproduction terial. We paid special attention to the latter two as (e.g., Minguez 1998, Reid et al. 2002, Hanssen et these entail potentially the most stressful and/or al. 2005, Heij et al. 2006). Therefore, knowledge costly behaviors and are directly related to parental on behavioral complexity during the incubation care (guarding, and improving conditions at the period appears crucial for estimating parental in- nest site). Assuming an equal contribution ofthe vestment ofmales and females both at that time parents in incubation duty (Stempniewicz & and also during the whole reproductive season. Jezierski 1987), we hypothesized that males, with Here, we investigated sex-specific patterns of an increased stress level during incubation (Jaku- parental care during the incubation period in the bas et al. 2008), would spend more time and/or Little Auk (Alle alle), a small, planktivorous sea- participate in more aggressive interactions and bird that breeds in rock crevices at coastal Atlantic collecting ofnest material than females, whose areas ofthe High Arctic region (Stempniewicz stress level decreased during incubation. 2001). Like many other seabirds, Little Auks are socially monogamous with negligible sexual di- morphism (Jakubas & Wojczulanis 2007). Both 2. Material and methods partners incubate the single egg and feed the chick, although females tend to cease chick feeding to- 2.1. Study area, field and laboratory work wards the end ofchick rearing, and males exclu - sively take care ofthe young (Stempniewicz 2001, The study was conducted at a breeding colony of Harding et al. 2004). Three studies have examined Little Auks at Ariekammen slopes (77°00’ N, sex differences in parental duties during the chick- 15°33’ E) in Hornsund, South in rearing period (Harding et al. 2004, Wojczulanis 2006. For detailed monitoring ofthe time spent in et al. 2006, Welcker et al. 2009), but relatively lit- and outside the nest and behavior performed out- tle is known about the parental activities ofeach side the nest during the incubation period, birds sex throughout the breeding season. To our were caught using mist nets or noose carpets knowledge, the only study focusing on Little Auk (pieces ofthick net with tiny monofilament loops incubation behavior found that both partners con- tied in “nooses” to capture the birds’ legs; Wil- tributed to incubation, but the sex ofthe studied liams et al. 2000), spread over the colony surface birds was unknown (Stempniewicz & Jezierski in a restricted sampling patch (hereafter the moni- 1987). Jakubas et al. (2008) demonstrated a differ- tored colony patch). ent pattern ofstress level, as expressed by The monitored colony patch was situated in the heterophil/leucocyte (H/L) ratio changes, in Little central part ofa colony, and the number ofbirds Auk males and females during the incubation peri- present on that patch was comparable with the od. The stress level in females decreased (higher neighboring areas. Before egg-laying, 55 individ- H/L ratio) with the progress ofthe incubation peri - uals were caught and marked individually (distinct 142 ORNIS FENNICA Vol. 86, 2009 color marks, dyed on breast feathers, and a combi- conducted on the 9th,15th,19th, and 27th day after nation ofcolor rings). A small drop ofblood from laying. Time spent inside the nest cavity and in the the brachial vein ofcaught individuals was taken vicinity ofthe nest (expressed further as territory and stored in 1 ml of96% ethanol forlater DNA- attendance) was calculated based on the pres- based sex identification. All birds caught were ence/absence ofmarked individuals on the surface adults (i.e., two years old or older; distinguished ofthe monitored colony patch watched continu - from subadults based on the appearance of flight ously and notied at least every 10 minutes. The ex- feathers and upper-wing coverts; Stempniewicz act time ofbirds entering and exiting nests and/or 2001). departures from and arrivals to the monitored col- The breeding status, partner and location ofthe ony patch were recorded. All occurrences ofag - nest entrances ofthe caught birds were defined gressive interactions and collecting nest material during 22 continuous watches (1–12 h) carried out were recorded and described in detail. Threaten- during the pre-laying and early incubation periods, ing, attacking and defending, expressed by charac- and during four 24-h continuous watches during teristic postures (upright position, tense body, the incubation period. Social pairs could be easily bristled head’s feathers) and/or mutual physical recognized as pair mates. They continuously stay contact, against other individuals were considered close together and copulate frequently with each aggressive interactions. The initiator and the re- other during the pre-laying period, and later on in ceiver ofeach aggressive interaction were re - the season use a shared nest. Extra-pair copula- corded. For occasions ofnest material collecting, tions are easily distinguished from within-pair the type ofitem (pebbles, lichen and moss pieces, ones, as females do not usually accept extra-pair etc.) and the success rate ofits delivery to the nest contacts and perform rejection behavior (Wojczu- were also recorded. The material was considered lanis-Jakubas et al. 2009). In total, we observed successfully delivered if a bird with item entered behavior of21 pairs with both partners marked, the nest cavity. and 13 additional individuals (7 males and 6 fe- To evaluate the importance ofthe incubation males) paired with unmarked partners. Nest sites period for the occurrence of the selected behav- ofall observed birds were situated in close prox- ioral patterns, surveys ofaggressive interactions imity, allowing two observers to reliably watch the and nest material collection by unmarked individ- whole colony that encompassed all the studied uals were performed. These surveys were con- birds. ducted during the three weeks preceding the egg Access to many nests was limited due to the laying, the whole ofthe incubation period, and for Little Auk nesting in rock crevices. To establish the first nine days of the chick-rearing period (ac- the timing of breeding for birds from the whole cordingtomediandataofegglayinginthein- monitored colony area, day-to-day examination of spected nests, established backwards for pre-lay- a group of67 nests was performed during the pre- ing period). laying period (4–15 June). The monitored nests All occurrences ofaggressive encounters and were situated in the part ofthe colony where birds carrying nest material in the bill were noted marked birds were observed and the surveys ofun - during 5-min continuous scanning ofthe area of marked birds were conducted. Seven ofthese 67 900 m2 with nests ofca. 300 pairs and with ca. nests were those ofmarked birds. The egg laying 200–300 birds observed during each survey. The was highly synchronous in the colony, 96% of monitored colony patch, with the marked birds, eggs being laid during four days (10–13 June), and was within the scanned area. Surveys were per- was completed in six days. Therefore, median date formed up to five times per day at different hours ofthe egg-laying (12 June) was considered as the to account for the potential influence of time of day first day of incubation for all marked and un- on bird activity. In total, 133 surveys (68, 52, 13 marked birds from the studied colony. Location of during the pre-laying, incubation and chick rear- the inspected nests was known from the previous ing period, respectively) were performed. seasons. The DNA for sexing was extracted from coag- Four continuous 24-h watches were performed ulated pieces ofblood (af ter the ethanol evapora- across the incubation period. The watches were tion) using the Blood Mini kit (A&A Biotechnol- Wojczulanis-Jakubas et al.: Parental care by incubating Little Auks 143

             

     

 

               

         

    

     

                      

Fig. 1. Time spent by Little Auk males and females (mean and SE) in the colony: in- and outside the nest and in the vicinity of the nest (territory attendance) during the incubation period in Hornsund in 2006. Num- bers above the diagrams indicate the number of observed birds. The arrows indicate significant sex differ- ences (paired t test). ogy, Gdynia, Poland). Subsequent molecular anal- 2.2. Statistical analyses yses were performed with the primer pair F2550 and R2718, according to Griffith et al. (1998), us- Intersexual comparisons ofthe time spent in- and ing 50° annealing temperature for the PCR reac- outside the nest were made only for pairs with both tion. These primers amplify a 430 bp fragment on partners marked using paired t-tests [N =21forthe the W chromosome for females only, and a 600 bp first three watches and N = 20 for the last watch; fragment on the Z chromosome for both sexes one nest was predated by the (Alopes (Fridolfsoon & Ellegren 1999). This size differ- lagopus)]. The data on time spent outside the nest ence was clearly visible when separating the frag- were logarithmically transformed before the anal- ments on a 2% agarose gel. ysis due to the slight divergence from the normal 144 ORNIS FENNICA Vol. 86, 2009

Fig. 2. Number of Little Auks in the monitored colony patch observed with nest material in bill during prelaying, incubation and early chick-rearing periods in Hornsund in 2006. distribution. To compare the diurnal rhythm ofin - and the difference was marginally significant also cubation ofboth sexes, the identity ofa bird incu - for the fourth watch (first watch: t = –3.60, P = 20 bating during the observation period (only for 0.002; second: t = –2.20, P = 0.04; third: t =– 20 20 pairs with both partners marked) was established 2.59, P = 0.02; fourth: t = –1.85, P = 0.08) (Fig. 19 every two hours during the four watches. The fre- 1). quency ofmale and female presence at the nest Aggressive encounters noted during the sur- during the 12 checks was compared using Chi- veys ofunmarked birds were observed relatively square test for the four watches combined. The fre- rarely during the incubation period (0.73 ± 0.09 SE quency ofaggressive behavior and occurrences of encounters per survey; N = 68) compared with the nest-material collecting were calculated for all prelaying period (1.74 ± 0.05 SE, N = 52; Mann- marked individuals and compared between sexes Whitney Z = 2.57, P = 0.01). During the incuba- using t-test for independent variables. To compare tion period, marked males and females partici- the frequency of aggressive encounters and occa- pated in aggressive interactions both as initiators sions ofnest-material collecting noted during sur- and receivers. Males initialized such interactions veys ofunmarked birds between breeding stages, more frequently than females (7.89 ± 1.13 SE and Mann-Whitney and Kruskal-Wallis tests were 2.60 ± 0.73 SE, respectively; t = –3.85, P = 53 used due to the heterogeneous variance ofdata. 0.0003). However, considering the number ofini - Descriptive statistics are expressed in the text as tialized aggressive interactions per time spent at mean and standard error. The critical alpha level the territory, sexes behaved in a similar way was 0.05. The statistical analyses were performed (males: 0.32 ± 0.04 SE and females: 0.24 ± 0.06 SE using STATISTICA 8.0. events per bird per hour; t = –0.98, P = 0.33). 53 Nest material collection during the survey, ex- pressed as the number ofunmarked birds carrying 3. Results nest material, was more frequent during the incu- bation period compared with pre-laying and chick Marked males and females spent similar amounts rearing periods (Kruskal-Wallis H = 28.70, N = 2 oftime in the nest cavity during the 24-h watches 133, P < 0.001; Fig. 2). Both marked males and fe- (first watch: t = 0.33, P = 0.75; second: t = 0.27, males participated in collecting nest material, but 20 20 P = 0.79; third: t = 0.43, P = 0.67; fourth: t = males were observed more often with nest material 20 19 0.51, P = 0.62) (Fig. 1). The frequency of male and in the bill (78% ofthe total of427 observations; ¤ 2 1 female presence at the nest cavity was similar dur- = 89.11, P < 0.001). However, most marked birds ing the 12 checks, performed every two hours dur- (all the males and 89% ofthe females; Fisher’s ex - ing each ofthe four24-h watches (¤ 2 test, ¤2 = act test, P = 0.85) were observed collecting nest 11 3.92, P = 0.97). Males attended the nest territory material. On average for these birds, the behavior more than females during the first three watches, occurred 17 ± 0.9 SE times (range 2–139). Sexes Wojczulanis-Jakubas et al.: Parental care by incubating Little Auks 145 were similar in terms ofthe frequencyofnest ma - (IGF, PAS unpublished data). These relatively terial collection attempts per time spent on the sur- constant environmental conditions may explain face of the monitored colony patch (males: 0.2 ± the lack ofdiurnal pattern in changes ofthe incu - 0.06 SE observations ofan individual with item bating partners. per hour, females: 0.3 ± 0.12; t = –0.54, P = 0.59). In seabirds, costs ofphysical activity while at - 53 The most often observed nest material items tending the territory are relatively higher than in- carried by marked birds were pebbles (males 62% cubation costs (Thomson et al. 1998, Tinbergen & ofthe collected items, N = 333; females 52%, N = Williams 2002). Little Auk individuals that were 94) followed by dry pieces of mosses and lichens not on incubation duty actively participated in ag- (males 37%; females 47%). The rest consisted of gressive interactions and collected nest material, bird sternum, dry goose faeces and grass blades. thereby also devoting their foraging time on paren- Both sexes collected particular types ofnest mate - tal care behaviors. Both sexes performed these be- rial with similar frequency (pebbles: ¤2 = 0.53, P haviours, yet males attended the territory more 1 = 0.47; and mosses and lichens: ¤2 = 0.88, P = than females. Consequently, the contribution of 1 0.35). The majority ofthe observations ofnest ma - males to duties was greater, which presumably is terial collection led to a successful delivery to the reflectedin the increase ofstress level ofmales nest, with similar success rates for males and fe- during incubation (Jakubas et al. 2008). The ap- males (76% and 75%, respectively; ¤2 = 0.01, P = parent unequal division oflabor between sexes 1 0.94). might be a consequence ofthe large female invest - ment during egg formation. There are no data on the costs ofegg production in Little Auks, but a 4. Discussion high energy expenditure could be assumed for auks. For example, egg formation in guillemots Both sexes incubated for about 12 hours per day, a costs 85% of female basic metabolism rate (refer- result similar to that observed earlier for the Little ences in Nettleship & Birkhead 1985). After the Auk and other auks (Stempniewicz & Jezierski costly egg formation females might be unable to 1987, Gaston & Jones 1998). Incubation bouts participate in the off-duty activities. Instead, they lasting about twelve hours in the Little Auk are may have to spend more time foraging to physi- presumably long enough to allow the off-duty par- cally recover. The longer staying ofmales in the ent to replenish its body reserves. Foraging flights colony during the incubation has also been ob- of Little Auks, performed to collect food for served in other species ofauks: forexample, Brün - chicks, may sometimes last only ca. 30 min but are nich Guillemot ( lomvia), (Alca usually 3–5 h (Harding et al. 2004, Steen et al. torda)(Paredeset al. 2006) and 2007, Wojczulanis-Jakubas 2007). Thus, it seems (Fractecula arctica) (Creelman & Storey 1991). plausible that adults are able to feed themselves This difference may result from males guarding during the few hours of their off-duty time during nests against disturbance from breeding and non- the incubation period. Indeed, the body mass of breeding neighbors. Physiological determinants males and females increased in the course of incu- such as higher levels oftestosterone (e.g., Ball & bation (Taylor 1994, Jakubas et al. 2008). Balthazar 2004, B³aszczyk et al. 2006), may make The daily rhythm ofincubation ofLittle Auks males better prepared and thereby become more were similar for males and females in the present efficient than females in nest defending. Hence, it study, although other studies have reported differ- would be beneficial for both partners if the male ences in staying frequencies for some auk species spent more time and effort defending the nest. An breeding in lower latitudes (e.g., Gaston & Jones alternative explanation for the higher territory at- 1998, Paredes et al. 2006). Little Auks, however, tendance ofmales might be that males had more breed in the High Arctic region, with the summer time than females for staying in the colony. Forag- months having 24-hour sunlight, little diurnal ing flights performed by males during the chick- variation in the availability ofzooplankton re - rearing period may be shorter than those done by sources (B³achowiak-Samo³yk et al. 2006) and females (Welcker et al. 2009). The causes ofthat relatively low variation in daily air temperature difference are unknown, but foraging areas or for- 146 ORNIS FENNICA Vol. 86, 2009 aging efficiency may be different between males such might be regarded as an important part ofpa - and females. Another possibility is that, during the rental care (Fargallo et al. 2001). incubation period, males might forage closer to the Subtle sex differences in parental care seem to colony or more effectively than females and there- be the rule for seabirds, and the Little Auk is not an fore might stay longer periods in the colony. exception. Our results suggest that parental care Although the aggressive behaviour ofLittle during the incubation period is slightly biased to- Auks was most pronounced during the pre-laying wards greater male participation. Higher stress period, it was still noticeable during the incubation level ofmales in that period (Jakubas et al. 2008) period and might play an important role in mani- suggests allocation ofresources fromthe immune festation of the site possession by the nest holder. function to parental care. Both male and female are High nest-site fidelity and long-term pair bonds likely to benefit from adopting sex-specific paren- (authors’ unpubl. data) may promote nest-site tal roles during incubation. Various parental strat- guarding for possible future seasons. Moreover, egies ofresource allocation in both sexes during nest-site guarding by off-duty partners may allow the incubation might be related to their specific pa- the incubating bird to remain undisturbed (Birk- rental roles and efforts, both at pre-laying and sub- head 1978, 1985). sequent stages ofthe breeding season. However, to Collection ofpebbles and other nest material understand the causality ofthe labor division be - by Little Auks was almost exclusively performed tween the sexes in Little Auk, further observa- during the incubation period. This is probably re- tional and experimental studies ofthe energy ex - lated with the fact that the species do not build a penditure ofboth sexes at the particular stages of true nest and only gathers items in the nest cavity reproductive cycle are needed. to improve conditions inside for the breeding sea- son. Pebbles may prevent the egg from rolling and Acknowledgments. We are grateful to Ann M.A. Harding crushing against the hard rock walls ofthe nest and two anonymous reviewers for their invaluable com- chamber (Ferdinand 1969, Stempniewicz 1981). ments and linguistic improvements on the manuscript. We Soft items, such as pieces of dry mosses and li- also thank Micha³ K. Kowalewski and the staff of the Pol- chens, might insulate the egg by limiting its con- ish Polar Station at Hornsund (Institute ofGeophysics, Polish Academy ofSciences) fortheir kind assistance and tact with bare nest floor, as suggested for Chin- hospitality during the field work. The project was sup- strap Penguins (Pygoscelis antarctica;Morenoet ported by a grant from the Polish Ministry of Science and al. 1995). The present results showed that collec- Higher Education (KBN 0640/PO4/2005/29). The study tionofnestmaterialwascommonandseemstobe was performedunder permission ofthe Governor ofSval - intentional – the majority ofitems were success - bard. fully delivered to the nest. In contrast, in Razor- bills and Common Guillemots (Uria aalge), nest- material collecting appears to be more ritualized, Sukupuoliriippuvainen investointi as the birds usually drop the pebbles on the ground vanhemmuuteen pikkuruokilla outside the nest (Bedard 1969, Birkhead 1976, Lloyd 1976, cited after Cramp 1998). It is difficult Sukupuolisidonnainen käyttäytyminen lajeilla, to estimate the costs ofnest material collecting by joilla molemmat puolisot osallistuvat poikasten Little Auks. Pebbles found in the inspected nests hoitoon, johtaa evolutiivisesti ristiriitaan suku- weighed on average 3.9 ± 0.48 SE g (N = 165; the puolten välisen työnjaon ja huolenpidon välillä. equivalent to 2.3% average body mass ofmales Tämä ristiriita saattaa olla vähäisempää lajeilla, and 2.4% offemales during the incubation; joilla on pitkäaikaiset parisuhteet. Tutkimme tätä Wojczulanis-Jakubas 2007). Thus, the mass ofa kysymystä haudonta-aikana yksiavioisella, yh- single pebble appears negligible. On the other dyskunnissa pesivällä, arktisen alueen merilinnul- hand, pebbles were transported in the bill, which is la, pikkuruokilla (Alle alle). Selvitimme sukupuo- beyond the central point ofthe body, sometimes leltaan tunnistamattomien yksilöiden pesässä ja for large distances, i.e., a few dozen meters. In sen ulkopuolella viettämää aikaa sekä ajankäyttöä Chinstrap Penguins, intensive pebble collecting tiettyihin tarkoituksiin (aggressiiviset kohtaamiset decreased the body condition ofindividuals and as ja pesämateriaalin keruu) neljän 24 tuntia kestä- Wojczulanis-Jakubas et al.: Parental care by incubating Little Auks 147 neen tarkkailujakson aikana. Koiraat ja naaraat ja- cess in birds: Simultaneous effects of age, pair-bond koivat haudontavastuun ja sen ulkopuolisen ajan duration and reproductive experience. — American tasaisesti. Koiraat kuitenkin oleskelivat naaraita Zoology 35: 318–328. Fridolfsoon, A. 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