post-fledging dispersal of common guillemots uria

103

POST-FLEDGING DISPERSAL OF COMMON GUILLEMOTS URIA AALGE GUARDING C HI CKS IN THE NORTH SEA : THE EFFECT OF PREDATOR PRESENCE AND PREY AVAILABILITY AT SEA KEES (C.J .) CAMPHUYSENI, 2 Camphuysen C .J . 2002 . Post-fledging dispersal of Common Guill emots Uria aalge guarding chicks in the North Sea : the effect of predator presence and prey availability at sea . Ardea 90(1) : 103-119 . Chick growth and mortality characteristics (including predation risk) have been considered key selective factors to account for the evolution of the intermediate fledging strategy in Common Guillemots Uria aalge . The semi-precocial young leave the colony as sma ll , partly feathered, flightless chicks at an age of c . 20 days at about one qua rter of adult body mass and are accompanied by one of the adults (usuall y the male) when they swim out to sea. It is generally assumed that morta lity rates in the colony are re latively low, while growth rates have been measured to be lower at the colony than at sea . Information on post-fledging dispersal of young an d adults at sea in late summer (late June-Septem ber) is evaluated in this paper . Adult guillemots from North Sea colonies guide their offspring away from the colony . While doing so, they move rapidly through a coastal area with rich prey resources but with relatively high predation ri sk, and travel several hundreds of kilometres into the open sea where there are ve ry few avian í' predators but where prey is low and patchy. Some were shown to end in dist ant areas with fewer predators and predictable prey resources . Mean while, the adults undergo a complete post-nup tial moult and become flightless for about 40-45 days . Laying, hatching and fledging in Common Guillemots are highly synchronised and with little variation in timing between years and very high success rates . In contrast, post-fledging chick surv ival is highly variable, which is understandable given the ri sky journey undertaken in often adverse environmental conditions . It is suggested that die selec~ tion pressure to defend or conquer breeding sites on proven successful ledg/ es in autumn ( starting only three months after `normal' fledging) may strongly select for a timely departure from the colony. Chick care at sea allows the parents to become flightless while they undergo post-nuptial moult in time so that they c an keep up with non-breeding adults and return to visit the breeding ledge in time . Key-words: Uria aalge - fledging - chick dispersal - parental care - North Sea - feeding conditions - predator presence - moult - nest site defence ' Netherl ands Institute for Sea Research (NIOZ), P.O . Box 59, 1790 AB Den Burg, Texel, The Netherl ands . E-mail camphuys@nioz .nl ; 2CSR Consultancy, Ankerstraat 20, 1794 BJ Oosterend, Texel, The Netherlands.

INTRODUCTION the parents . The unique variability in chick development and juvenile life histories in Alcidae proCommon Guillemot Uria aalge chicks leave the vides and attractive context in which to explore breeding ledges while still flightless (semi-preco- trade-offs in the parent-offspring conf lict, where cial young), at a quarter of adult body mass, and the chick's and the adult's perspectives may select swim out to sea, usually accompanied by one of for opposing strategies (Lack 1968 ; Cody 1971 ;

104 ARDEA 90(1), 2002

Ydenberg 1989; Birkhead & Harris 1985 ; Gaston feeding both when the energetic requirements of & Jones 1998) . Hypotheses for the evolution of the chick increase . If chick safety and chick proviparticular fledging modes have suggested that sioning should be optimised, parents should guide chick growth and mortality characteristics are key their offspring at sea into areas with ample supselective factors (Birkhead 1977a ; Ydenberg 1989 ; plies of suitable prey and few predators interested Gaston & Jones 1998) . Suggested selection factors in guillemot chicks, or where adults can adequatein Common Guillemots include the presence of ly protect the chick . When the chicks are proviterrestrial predators, reduced load-carrying capac- sioned at the colony, parents exploit particularly ity of the adults (large size, small wings), cliff rich and preferably nearby foraging areas, to minnesting (precocial departure impossible), open imise the time spent away from the colony (Pearnest site (chick guarding required) and distant for- son 1968 ; Cairns et al. 1987; Monaghan et al . aging. Ydenberg (1989) considered the fitness 1994) . A first prediction would therefore be that costs and benefits of the breeding site and the parents guide their fledged chicks towards these open sea, suggesting that there is an optimal time `known' areas . Secondly, one could expect that for the developing chick to leave the ledge and adults, just as in the colony and to protect the jump into the ocean . chick against (avian) predators, establish a posiIt is not clear whether chick or parent(s) initia- tion for their chicks centrally in areas of high te departure (Tuck 1960 ; Swennen 1977), but the guillemot abundance . Here the many surrounding entire colony is extremely noisy when the time individuals would buffer them from predators comes (Tuck 1960 ; Daan & Tinbergen 1979) . (dilution effect; Weatherhead 1983 ; Elgar 1989 ; Chicks leave the colony while they are still sever- Creswell 1994, Alcock 1997), just as in the coloal weeks away from being independent and able ny (Birkhead 1977b) . More eyes in a large flock of to fly. Prior to departure, at about three weeks of conspecifics may increase predator detection, and age, the chick's body mass increase tapers off and the sheer number of birds may decrease the indireaches a plateau around 250g, while wing length vidual risk or predation . I will test the two prediccontinues to increase (Johnson 1944 ; Mahoney & tions using field data on the distribution and behaThrelfall 1981 ; Gaston 1985 ; Harris & Wanless viour of Common Guillemots (and their off1988 ; Harris et al . 1991) . Birkhead (1977a) sug- spring), their predators at sea and their feeding gested that the young bird should have an ade- activities just prior to, during and after departure quate wing surface/mass ratio, to increase the dis- to sea, in an attempt to understand the behavioural tance they can glide when they jump and then strategy of Common Guillemots during postdive immediately to avoid predatory gulls, i .e . a fledging dispersal. suitable compromise between aerial and underwater 'flight' . He indicated that the energetic requirements of the (growing) chick at the cliffs METHODS would ultimately exceed that which its parent s (could) obtain and transport. Study area There is remarkably little published informa- This study covers the western North Sea (53tion on the dispersal of Common Guillemot 59°N ; 4°W-5°E; Fig . 1), an area of approximately chicks at sea. Harris et al . (1991) found that after 272 000 km2, with locally very large numbers and leaving the colony, chicks grow faster than during a great variety of seabirds (Skov et al . 1995 ; Stone the fmal colony period . It has been shown that et al. 1995 ; Camphuysen & Webb 1999). Breeding colony life is relatively safe (Harris & Birkhead colonies of Common Guillemots occur scattered 1985 ; Ydenberg 1989), but the risk of predation of along the English and Scottish coast (Lloyd et al. the unguarded chick on the ledge could be exacer- 1991) . The advantage of this study area is that it is bated by the prolonged absences of the parents a`simple' area (colonies on one side, open sea on

POST-FLEDGING DISPERSAL OF GUILLEMOTS GUARDING CHICKS 105

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106 ARDEA90(1), 2002

5s°tv

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Fig. 1. Study area and 17 large N breeding colonies of Common Gui lle° ti mots along the Eng lish and Scottish east coast (after Lloyd et al. 1991) ~°N used to assess `distances to the nea rest colony' . The dotted line roughly indiSCOTLAND

56°N ~

55

cates the transi ti onal zone between mixed coastal water and thermally stratified central North Sea water . Frontal boundaries may be expecte d CE wrRA EA at varying locations around the dotted ~ line (from Pingree & Griffiths 1978 SJm -. and personal observ ations 1987-99) .

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the other side), with a relatively straightforward to calculate densities (n knr2) . Flying birds were oce anography. Thermally mixed coastal water is included in the transect according to the snapshot separated from thermally stratifi ed central North method . All birds, whether swimming or flying, Sea water by a tran sition zone roughly parallel to that operated `together' or stayed tight in a particthe coast off Scotland (Aberdeen Front) and Eng- ular area or in a particular movement were marland (Flamborough Front), with extensions into ked as distinct `flocks' . Flocks comprising more the Southern Bight (Frisi an Front) (Pingree & than one species were named `multi-species Griffiths 1978; Lee 1980 ; Otto et al. 1990) . (feeding) associations' (MSFAs ; Camphuysen & Webb 1999) . Older data needed to be re-proField observations cessed, so that details of ( foraging) behaviour in Ship-based surv eys were conducted using the obse rved seabirds, as they were scribbled o n strip-transect counts, which were developed as a the margins of the o riginal recording forms, could standard for the North Sea (Tasker et al . 1984). be entered into the database . Simultaneously durCounts were conducted outside, from the top- ing transect counts, a 180° scan of the area ahead deck of the ship during steaming by one or two of the ship is genera lly used to record scarcer speobservers, operating a 300 m wide transect on one cies during ship-based surveys, again fo llowing side and ahead of the ship . Birds were normally methods described in Tasker et al . (1984). The discovered with the naked eye and identi fi ed 180° scan was here used to enlarge the sample of using binoculars . St andards counting units were feeding frenzies and MSFAs which is used to 10-minute periods and all swimming birds or examine species and age composition as well as birds touching the water within transect were used foraging behaviour (Camphuysen & Webb 1999) .


Such data were not used to calculate densities, but and razorbills Alca torda), and feeding Atlantic were presented as relative abundance estimates (n puffms Fratercula arctica and attracted a whole km-1 travelled) . suite of surface feeding piscivorous seabirds .

`Father-chick combinations' (adult auks Active MSFAs were considered indicative of accompanying a small, flightless chick or fully- good feeding opportunities, and hence, better pregrown young) were specifically coded . During dictors of prey availability than stock assessments late summer surveys 1997-99, guillemot chick through acoustic surveys (i .e . presence of fish records included a rough indication of chick size shoals) . Distances to breeding colonies were (code 1= chick less than half adult size, 2 = half assessed by calculating the distance (km) of each to near adult size, 3 = adult size) . In August and record to the nearest of 17 of the largest guillemot September it is increasingly more difficult to colonies or groups of colonies along the English identify chicks, because these are now fully and Scottish east coast (c . 98% of all nesting grown while the adults have moulted into winter Common Guillemots between 54-59°N, Fig . 1 ; plumage. Adults undergo a complete post-nuptial after Lloyd et al . 1991) . In the analysis, sightings moult and shed the primaries simultaneously were grouped in 10 km wide bands (0 km = 100 53°N

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Fig. 2 . Distribution of father-chick combinations (n km- ' ) in June, July, August and September. Open circles indicate quadrants with surv ey effo rt, but with no sightings . phuysen & Webb 1999), the median distance of (37.7% of all birds, n = 68 497), usually feeding which was found at approximately 30 km from in associati on with Common Guillemots (27 .6% nearest guillemot colonies . 90% of all MSFAs of all birds) . The median distance of actively forwere found within 90 km of the guill emot colo- aging fu lly grown Common Gui llemots in July nies and these flocks were numerically dominated was at 30 km from the nearest colony (90% withby Black-legged Kittiwakes Rissa tridactyla in 60 km of the colonies ; Fig. 4) . The median of

110 ARDEA 90(1), 2002

100 Fig . 3 . Relative abundance of `father-chick combinations' and 0.8 proportion very small chicks 80 I 0•7 é (about half adult size) with 0.6 increasing distance to the nearest 60 colony (km) in July. Y 0 .5 m 0 .4 QY 0 .3 -7 °c~i 0 .2 0 .1 0 .0

y

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0 ~ -Tl`,I IÌ iffTI`~i i'f C i ilI i I --i i i 0 50 100 150 200 250 300 350 distance to nearest colony (km )

100 Fig. 4. Relative abundance (n km-1 travelled) of fally grown 0.7 80 Common Guillemots and propor0) .6 á, tion actively foraging individuals 0 co 0 (%) with increasing distance from Y 0 .5 60 the nearest colony in July. A black m 0 .4 F1 arrow indicates median distance 40 of all actively foraging guille~ 0 .3 . L Y mots, a shaded arrow indicates the 0 0 .2 I 20 m medi an dist ance of all guillemots . 0-0 1 0 .1 I ' ~ 0 0 n 0 .0 i 0 50 . 100 150 200 250 300 350 distance to nearest colony (km) 0.8-

all fully grown guillemots, irrespective of behavi- s andeels), but more convincingly by the frequent our, occurred at 40 km, 75% were found within 90 occurrence of actively feeding Common Gui ll ekm, 90% within 150 km from the colonies . Of all mots, usually foraging socially, apparently d rivguill emots flying towards land with fish, 98 .2% ing small shoals of fish towards the surface during were seen within 60 km from the colonies (93 .8% a simultaneous dive ( Camphuysen & Webb 1999). within 40 km) . Father-chick combinations were never seen t o Group size of foraging Common Guill emots at actively join these feeding frenzies . Most foraging sea was most variable within 80 km from the activity ceased at the seaward side of a frontal nearest colony ( Table 2) . A total of 46 aggrega- zone running parallel along the B ritish east coast . tions of over 100 Common Guillemots were This front occurred at increasing distan ce away recorded (max . 1547 individuals), 5 of which from the coast in August and September (usually were found to include chicks ( 1, 12, 19, 36, and within 80 km from the coast) and formed the tran 51 chicks) . At greater distances, groups are small - sition zone between thermally stratified, clear er an d large aggregations did not occur ( 80-300 water of the central North Sea and mixed water km ; max . 38 individuals group-I , average 2.5 ± along the coast . Central North Sea waters were very poor in surface shoaling fish, but mid-wate r 0.2, n = 213) . Feeding areas were characte ri sed by the fre- shoals of gadoid and clupeoid fish were encounquent occurrence of fish shoals (clupeoids and tered occasionally (30-70 m depth) . MSFAs and


Table 2 . Flock size of actively foraging Common Guillemots and father-chick combinations (average ± SE an d max . flock observ ed) with increasing distan ce from the nearest colony. Average = derived mean (back-transformed to original scale after log-transformation of the data) . Feeding Guillemots Father chick-combinations Distanc e (km) Flocks (n) average SE maximum Flocks (n) average SE maximum 10 195 6 .6 ± 0.3 110 78 2.5 20 197 4 .6 ± 0 .2 71 291 2.9 30 258 4 .8 ± 0.2 200 483 2.7 40 269 5 .0 ± 0.2 308 484 2.7 50 225 6 .6 ± 0.3 1547 405 2.7 60 178 7 .6 ± 0.3 748 427 2.6 70 129 4 .1 ± 0.3 470 442 2.5 80 99 8 .3 ± 0.5 400 319 2.4 90 94 3 .4 ± 0.3 38 458 2.6 100 21 3 .4 ± 0.7 30 249 2.4 110 5 2 .6 ± 0.8 4 187 2.3 120 15 1 .8 ± 0.9 24 175 2.3 130 10 1 .2 ± 0.4 2 131 2.5 140 12 1 .3 ± 0.5 4 100 2.3 150 5 5 .1 ± 0.5 6 135 2.4 160 8 1 .3 ± 0.6 5 143 2.4 170 5 1 .9 ± 1 .0 7 132 2.5 180 142 2.4 190 5 1 .9 ± 0.7 3 98 2.2 200 5 2 .0 ± 0.9 4 99 2.2 210 14 1 .1 ± 0.4 3 88 2.2 220 2 1 .0 ± 0.7 1 54 2.5 230 27 2.3 240 6 3 .8 ± 2.0 28 13 2.4 250 4 2 .1 ± 0.8 3 18 2.3 260 2 2.0 270 3 2.0 280 1 1 9 2.2 290 1 5 4 2.0 300 3 2.0

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0 .2 47 0 .1 268 0 .1 80 0 .1 173 0 .1 99 0 .1 44 0 .1 21 0 .1 13 0 .1 139 0 .1 75 0 .1 11 0.1 11 0.1 13 0.1 9 0 .1 23 0 .1 9 0.1 15 0.1 18 0.1 6 0.1 6 0.1 6 0.2 15 0.3 8 0.4 4 0.3 3 0 .7 2 0.6 2 0.4 4 0.5 2 0.6 2

other feeding frenzies, including cetaceans, were as off the B ritish east coast, indicated by the presfound around the Dogger Bank and further east, ence of active MSFAs (Fig . 5) . The medi an disbut isolated sightings were scattered over a vast tance of potential predators in July, when gui llearea, suggesting that prey occurrences were mot chicks were small and most vulnerable, unpredictable and extremely patchy . occurred at 40-50 km from the nearest colon y

(75% within 140 km, 90% within 210 km) . In the Predator abundance central North Sea, densities of predators were Numbers of Great Black-backed Gull s and very low (< 0 .05 km-1) . Great Skuas were highest in the main feeding are-

112 ARDEA90(1), 200 2

Table 3 . Frequency of father-chick combinations (number of adults versus number of chicks per flock) at sea (n = 6460 flocks). chicks adults

1

2

3

4

5

6

>7

%

0 0.1 0 .0 0 .0 0 .2 1 74 .1 0 .0 0 .0 74 .1 2 7 .7 7 .7 0 .0 0.0 15 .4 3 2 .2 1 .0 1 .2 0 4 .4 4 0 .9 0 .4 0.3 0.3 1 .8 5 0 .5 0.2 0.1 0.0 0.1 1 .0 6 0 .2 0.2 0.1 0 .0 0.0 0.1 0 .0 0 .7 7 0 .4 0.1 0.0 0 .0 0.0 0 .0 0.6 8 0 .1 0.0 0.0 0 .0 0.2 9 0 .1 0.1 0.0 0 .0 0 .0 0.2 10 0 .0 0 .0 0.1 11 0.1 0.0 0.0 0 0 .0 0 .0 0.2 >_12 0.3 0.1 0.1 0.0 0 .1 0 .1 0.5 1 .2 %

86.6 10.0

1 .8

0.5

0 .3

0 .1

0.7 100.0

.0e • Nursery areas • . The only evidence of a nursery within the study area was found in the southeastern North Sea, E 0 .06 at approximately 53°30-54°30'N, 3°-5°E, c . 300 • km from the nearest colony of Common GuilleQ 0~ • ' mots . At the southernmost extension of the same frontal zone as is running along the British east CD 0

coast, between the 30 and 50 m depth a contour y=0 .7e14X-0.0045 ('Frisian Front') . Small chicks arrived as early as R2-o .n2s • 30 June, and the area had local densities of up to 0 .00 0.4 father chick-combinations km 7 2 . Flock size of 0.00 0.02 0 .04 0 .06 0.08 0.10 0 .12 father-chick combinations in July was low, on Great Skuas and Great Black-backed Gulls per km 0.02

average 2.9 ± 0 .3 (n = 48, max 12 adults with 5 . Correlation between the relative abundance (n chicks), but higher than expected from the graduFig. 5 krn-I travelled) of the main avian predators of Common al decline in group size with increasing distance to Guillemot chicks (Great Black-backed Gull and Great the colony (expectation 2 .03 ; Table 2). Flock size Skua) versus relative abundance of multi-species feed- declined further in August and September (2.7 ± ing frenzies (MSFAs) indicating utilised foraging 0 .2, n = 9; 2 .3 ± 0.6, n = 5 respectively). Predator opportunities of auks off the British coast . Individual presence was very low in June (0 .03 km-1), July plots represent n km-t travelled within 10km distance (0 .05 km-t), and August (0 .08), but increased bands around the nearest Uria colony (0-300 km) . markedly in September (0 .21 km71) (compare Fig . 5) . Most other father-chick combinations left the study area heading east, apparently crossing the North Sea and the remainder stayed in nearshore


Table 4 . Head moult in Common Guillemots with and without chicks at sea. B = breeding plumage, T = transitional plumage, W = winter plumage .

1-15 Jul 16-31 Jul 1-15 Aug 16-31 Aug B T/W %moult B T/W %moult B T/W %moult B T/W %moult with chicks 7092 230 3 .1 1492 50 3 .2 153 185 54 .7 34 408 92 .3 without chicks 5762 2063 26 .4 364 160 30.5 61 84 57 .9 46 646 93 .4 Gadj 1805 .62 271 .09 0 .42 0.44 P < 0 .001 0 .001 n.s . n.s .

100DISCUSSION

0

$o Post-fledging dispersal

Common Guillemots accompanying their off0 60spring (father-chick combinations) travelled right through the feeding areas that had been exploited as 40during the cliff-nest phase . The eastward disper~ sal was rapid and chicks were not led into the Q- 20 Mt, chicks feeding frenzies . Unlike anything superficial o without chicks more logic al , father-chick combinations went for

o

1-15 July

16-31 July

_j I

1-15 Aug

16-31 Aug

-J

their own areas, far away from the known nearcolony feeding grounds . Offshore father-chick combinations, except in the presumed nurse ry around the Fri sian Front and perhaps except on a

Fig. 6. Moult in fully grown Common Guillemots few occasions in clusters of birds on the British with and without chicks at sea (% winter or transitional (land) side of the frontal zone along the coast, were always swimming in an easterly or southplumage) per two-week period .

easterly direction . Especially in June and July, waters that were not clearly different from feeding when the chicks are still small, the eastbound disareas exploited by moulting adults that did not persal was fast . Assuming that the first chicks stay near chicks. depart around 24 June (Harris & Wanless 1988), a daily rate of movement of 50 km would have been Moult reached. In the early phase of chick departure (1-1 5 July), 3 .1% of adults accompanying chicks were Predator avoidance in transitional or winter plumage (n = 7322; Table Breeding success of Common Guillemots is 4) . A significantly greater fraction of fully grown highest on the densest ledges, largely because guillemots without chicks at sea showed active such birds suffer fewer losses from predators moult (26 .4%, n = 7825 ; Gadj = 1805 .6, df = 1, P (Birkhead 1977b) . A similar strategy could work < 0 .0001) . The difference in moult stage between at sea : larger flocks would automatically have guarding and non-guarding guillemots declined more individuals on the look-out for predators, late July and disappeared in August (Table 4, Fig . while the diluting effect would reduce the individ6) . ual risk. However, father-chick combinations did

114 ARDEA 90(1), 2002

not recruit to large flocks, which does not provide with some 35 000 fully grown individuals (possupport for the second prediction . In fact there sibly including some overlooked, èarly' fully was a tendency to spread out and reach very low grown chicks ; Camphuysen & Leopold 1994) . At densities over vast areas with eventually on aver- the nursery, flock size was slightly higher than in age just over one adult guarding an individual the area of transit . Avian predator presence was chick. The rapid dispersal into the open sea, away very low despite some favourable and predictable from the feeding frenzies of fully grown, social feeding conditions and local commercial fisheries foraging conspecifics and most other piscivorous (Leopold 1991), seals were absent or very rare . A seabirds (Camphuysen & Webb 1999), brought sample of guillemots shot under license in early them into areas that had a tenfold lower abun- autumn 1989 confinned that adults accompanying dance of avian predators than the coastal feeding chicks were indeed males . These auks had been areas just abandoned (Fig. 5) . Hence, post-fledg- feeding on sprat Sprattus sprattus and scad Traching dispersal meant they spread inconspicuously urus trachurus (Geertsma 1992), fish prey that are in small flocks over a vast surface area of water. known to occur concentrated along that transition The fact that chicks are capable of underwater zone between the Central North Sea and the flight immediately after their departure from the Southern Bight . However, within the study area, colony could then be the mechanism for individu- this was the only region that would qualify as a al escape. A look-out of on average just over one nursery . Although the study area was vast adult per chick, plus a quick response, may suffice (>270 000 km2), most father chick-combinations in areas with low densities of predators . One rea- left by crossing the North Sea at its widest point, son for parents accompanying chicks to avoid are- towards the Skagerrak (Denmark) and the Geras of high density and feeding frenzies could be man Bight (cf . Stone et al . 1995; European Seabecause large flocks of birds are conspicuous and birds at Sea database unpubl . material) . In the may thus attract predators (Eiserer 1984) that will Skagerrak area, there is a rapid build-up of Comgo for the least experienced flock members, the mon Guillemot numbers in late summer and early chicks . autumn, indicating the presence of more nurserie s Unfortunately, there are no data on the pres- at between 500 and 700 km away from the coloence and spatial differences in abundance of nies . underwater predators, such as large predatory fis h or marine mammals . Seals, known to prey at least Chick age and timing of departure occasionally on seabirds (Hamilton 1946 ; Bod- Chick mortality at the colony is highest in the dington 1978 ; McCanch 1981), were most abun- first days of the chick's life, mainly due to falling dant in coastal waters up to the frontal zone with off ledges, exposure, washing off, falling into most seabird feeding frenzies (ESAS database cracks, and other mishaps ('ilick 1960; Harris & unpubl. data) . It could be speculated that most lar- Wanless 1988; Harris et al . 1992) . After that, the ge predatory fish occurred in that same region, colony seems a rather safe place (Harris & Birkpreying on abundant (smaller) fish shoals . head 1985 ; Ydenberg 1989) and the decision to jump off the ledge would clearly put the not fullyNurseries grown chick at a greater risk again . Laying, hatchThere was some evidence for the development ing and fledging are highly synchronised (Harri s of a (small) nursery at a great distance from the & Wanless 1988). Typically, in the ten days after colonies . At the Frisian Front area (300 km south- hatching a young guillemot gains mass rapidly, east of the nearest colony), chicks would arrive but the rate declines then markedly so that by the from late June and on . Although overall concen- time it leaves (aged 18-23 days) the weight of an trations of birds seemed rather low, it was calcu- individual is more or less constant (Harris et al. lated that around 10 000 chicks occurred in July, 1992) . For colony departure, 14 June and 11


August were recorded as extreme dates around a Wanless 1988) . However, the number of young median (± SD) fledging date of 1 July ± 6 .3 days guillemots ringed on the Isle of May (Firth of (24 June- 7 July) . Forth) known to have survived to the following 1

Departure may be delayed until the stage that January, varied in six years between 12% and the chick is structurally so far developed that they 47% (Harris et al . 1992) . Obviously, the prospects can glide far and may avoid predation by diving for survival for chicks crossing the North Sea in immediately if necessary (Birkhead 1977a) . Struc- an easterly force 6 or in a hot summer with flat tural growth does not stop just prior to fledging calm weather is likely to be different. Harris et al . and we may anticipate a hunger stimulus in the (1992) demonstrated that survival of young chick to leave a place that is now less attractive . (expressed as recruitment into the colony after Interestingly, however, chicks raised in captivity some years of absence) declined significantly (in the absence of parents and with food ad libitwith hatching date in three out of six years of stuurn) initiate 'departure behaviour' at 15-21 days dy (no difference in the other years) . Highest surold (Swennen 1977) . The chicks became decided- vival (47% of the 1986 cohort) coincided with a ly restless by that age and sometimes refused winter (1986/87) in which exceptionally low morfood . Birkhead (1977a) observed a maximum of 7 tality of juvenile Common Guillemots was found chick feeds day 1 in Common Guillemots, provid- in a monitoring programme in the Southern North ing a chick with a mere 62 g of fish (adult mainte- Sea (C .J. Camphuysen, unpubl . data) . Thus sucnance requirements c. 200 g day-1) . It is difficult cess may not just have been a favourable `postto believe that guillemot parents cannot do any fledging' phase but rather the consequence of a better than this. Mathematical modelling by favourable winter. Houston et al . (1996) suggested that Brunnich's Quite intriguing is the fact that the chick is led Guillemots Uria lomvia are potentially capable of right through favourable feeding areas in which rearing a fully grown chick at the breeding site, feeding frenzies with guillemots are actually provided that they can find sufficient food nearby . ongoing, attracting large numbers of seabirds with Guillemots in Shetland, during a time when many similar prey . Camphuysen & Webb (1999) descriseabirds came in distress due to recruitment fail- bed the foraging behaviour of these birds, notably ures in sandeels in the late 1980s, were among the Common Guillemots, in these waters in considerfew species of seabirds that did not suffer bad able detail and concluded that many are engaged losses . These birds simply increased their time in social foraging : small groups herd fish shoals spent away and distance foraging to provide the towards the surface . If social foraging in guillechick in a way not too different from òrdinary' mots is a prerequisite to obtain sufficient prey in years (Monaghan et al . 1994) . Whether or not par- these waters, the area may not at all be that ents were incapable of further provisioning, or did favourable for young chicks that are frequently not attempt to do so, chick growth at sea immedi- left alone by most fully grown guillemots around ately following departure was better than during them . One can only speculate on these matters the final colony period. Harris et al. (1991) found and further research on the foraging strategies of that after leaving the colony, chicks gained mass Common Guillemots is recommended . at 15 g day-1, a growth rate equalling the rapi d mass gain in the first phase of chick development The adaptive value of intermediate departure on the ledge . ( 1) : the chick's perspective The picture emerges of a relatively safe coloSurvival at sea ny with consistently high hatching and fledging Hatching and fledging success in British Com- rates, but with a limitation on provisioning rates . mon Guillemots is generally very high and with Few of the suggested factors selecting for interrelatively little variation between years (Harris & mediate chick departure listed in the introduction

116 ARDEA 90(1), 2002

of this paper seem to be convincing after listing post-nuptial moult in comparison with other all the (potential) dangers to be met at sea, except guillemots at sea. Is it the need for the adults to if the chick would starve to death when it does not return in time to the colonies, to defend or conleave the colony in time. The costs of leaving at quer a site on a`successful' ledge, and thus to early age are quite clear: an increased risk of pre- maximise future reproductive success, that is dation, the low capability to cope with adverse most likely to select for the intermediate deparconditions at sea, and the immediate pressure to ture of their chicks ? swim several hundreds of kilometres into the blue. These costs must be outweighed by a benefit It is obvious that several questions still remain . . . . but what benefit? For example, how typical is the early autumn Apparently, the chick grows better at sea than return of adult guillemots as it is known to occu r during its fmal stay in the colony (Gaston & Net- at the very south end of their breeding range for tleship 1981 ; Ydenberg 1989 ; Gaston & Jones guillemots elsewhere? Or, how important is the 1998). A positive effect of early breeding (= early chick-rearing phase at sea covering a large area in departure) is documented, but not without diffi- terms of gaining experience and training in foragculty and the effect is not always that clear (Harris ing under different conditions under guidance by et al . 1992) . Chicks and their parents seem to rush one parent from the chick's point of view? Is is off, thinly dispersing over large areas at first, perhaps the problem of recognising the own offtowards distant nurseries and meanwhile ignor- spring that stimulates parents to bring their chicks ing, or very briefly taking advantage of, rich feed- into areas of low densities . Or, if males need to ing areas nearby the colonies . Part of the rush moult quickly and therefore move to sea, why do seems to be to avoid an area comparatively rich in female parents continue to frequent breeding avian predators . Why would an early participation ledges for some time after the fledging of their into such a rush be beneficial? In fact, if the chick offspring? Most these questions cannot be addreswas allowed to grow a little further, it would at sed with the (new) material provided in the preleast physically be slightly better capable to with- sent study. However, the post-fledging dispersal stand attacks from (avian) predators in the risky of chicks at sea, as described here for Common coastal zone . Guillemots in the North Sea, is clearly a crucial and risky phase during chick rearing that deserves The adaptive value of intermediate departure more attention in attempts to explain the fledging (2) : the parent's perspective strategy in auks . Raising a chick on the ledge would mean a continuation of the necessity to commute between foraging areas and the colony and primary moult ACKNOWLEDGEMENTS would have to be delayed . This could present a problem as successful breeders return to the colo- Field observations were carried out by Joke Bakker, nies in October to compete for the best sites and to Hans van Berkel, Kees Camphuysen, Lo Camps, Phimaintain the pair bond (Harris & Wanless 1989) . lipp Derks, Mark Hoekstein, Ico Hoogendoorn, Joslyn The need to return in time to the colony could Hooymeyer, Guido Keijl, Ben and Bert Knegtering, strongly select for the adult to bring the chick out Eduard Koopman, Marcel Laks, Mardik Leopold, : wing moult can now take place without Sander Lilypaly, Jaap van der Meer, Henk Offringa, Jan to sea any hindrance and at least a month earlier than den Ouden, Theo Postma, Jan Seys, Andy Webb, Marcus Werner, Louis Witte, Richard Witte and Pim Wolf. when the chick had to be provisioned on the led- Multi-disciplinary surveys on board RV Tridens in ge. The data on moult progress shown in this 1997 and 1998 were conducted with final support of the paper support this : at the time of chick-departures European Commission (EC DG XIV MIFOS project in early July, parents are clearly running late with 96/079). All collected data are deposited in the Euro-


pean Seabirds at Sea Database (ESAS) . I would like to Creswell W. 1994 . Flocking is an effective anti-predathank captains and crews of the various research ves- tor strategy in Redshanks, Tringa totanus . Anim . sels for their hospitality and co-operation on board and Behav . 47 : 433-442. cruise leaders Ad Corten and Bram Couperus for spe- Daan S . & Tinbergen J . 1979 . Young guillemots (Uria lomvia) leaving their arctic breeding cliffs : a daily cific help with the interpretation of acoustic signals collected during the transects . Mardik Leopold, Jaap van rhythm in numbers and risk . Ardea 67 : 96-100. Eiserer L.A . 1984. Communal roosting in birds . Bird der Meer, Theunis Piersma, Beth Scott and Andy Webb Behav . 5 : 61-80 .

all participated in fruitful discussions and support dur- Elgar M .A. 1989. Predator vigilance and group size in ing this study . I would like to thank Rob G . Bijlsma, mammals and birds . Biol . Rev. 64 : 13-33 .

Stefan Garthe, Mike P. Harris, Falk Huettmann, Bill Gaston A .J . 1985 . Development of the young in the Montevecchi, Theunis Piersma, Sarah Wanless, Ron C . Atlantic Alcidae. In : Nettleship D .N . & Birkhead Ydenberg, and two anonymous referees for stimulating T .R . (eds) . The Atlantic Alcidae : 319-354. Academand constructive comments on the manuscript . ic Press, New York. Gaston A .J . & Jones I .L. 1998 . The Auks . Bird Families of the World 4. Oxford Univ. press, Oxford . .J. & Nettleship D.N. 1981 . The Thick-billed REFERENCES GastonMurres A of Prince Leopold Island . Canadian Wildlife Service, Monographs Series No . 6, Ottawa. Alcock J. 1997 . Animal Behavior : an evolutionary Geertsma M . 1992. Dieet van de Zeekoet Uria aalge op approach . Sixth edition, Sinauer Assoc ., Sunder- het Friese Front in het najaar van 1989 ; een vergeland. lijkend voedselonderzoek . MSc thesis, Groningen Anonymous 1989 . Report of the Herring assessment University, Groningen . working group for the area south of 62°N . ICES Hamilton J.E . 1946 . Seals preying on birds . Ibis Jan. CM 1989/Asess :15 . 1946: 131-132 . Birkhead T.R. & Harris M.P. 1985 . Ecological adapta- Harris M .P. & Birkhead T.R . 1985 . Breeding ecology of tions for breeding in the Atlantic Alcidae . In : Net- the Atlantic Alcidae . In : Nettleship D.N. & Birktleship D .N . & Birkhead T.R . (eds). The Atlantic head T .R . (eds) . The Atlantic Alcidae: 156-204. Alcidae : 205-231 . Academic Press, New York . Academic Press, New York . Birkhead T.R . 1977a . Adaptive significance of the nest- Harris M .P., Halley D. & Wanless S . 1992. The postling period of guillemots, Uria aalge . Ibis 119 : 544- fledging survival of young guillemots Uria aalge in 549. relation to hatching date and growth . Ibis 134: 335Birkhead T.R . 1977b. The effect of habitat and density 339 . on breeding success in the Common Guillemot Harris M.P. & Wanless S . 1988 . The breeding biology (Uria aalge) . J . Anim. Ecol. 46 : 751-764. of guillemots Uria aalge on the Isle of May over a Boddington D . 1978 . Predations of seabirds by seals . six year period . Ibis 130 : 172-192 . Scott. Birds 10: 66-67 . Harris M .P. & Wanless S . 1989. Fall colony attendance Cairns D.K ., Bredin K.A. & Montevecchi W.A. 1987 . and breeding success in the Common Murre. ConActivity budgets and foraging ranges of breeding dor 91 : 139-146 . Common Murres . Auk 104: 218-224 . Harris M .P., Webb A . & Tasker M .L . 1991 . Growth of Camphuysen C .J . & Leopold M .F. 1994. Atlas of sea- young guillemots Uria aalge after leaving the colobirds in the southern North Sea . IBN Research ny . Seabird 13 : 40-44. report 94/6, NIOZ-Report 1994-8, Institute for Houston A .I ., Thompson W.A . & Gaston A.J. 1996. The Forestry and Nature Research, Netherlands Insti- use of a time and energy budget model of a parent tute for Sea Research and Dutch Seabird Group, bird to investigate limits of fledging mass in the Texel. Thick-billed Murre . Functional Ecology 10 : 432Camphuysen C .J . & Webb A . 1999. Multi-species feed- 439. ing associations in North Sea seabirds : jointly Johnson R.A. 1944. Weight records for some Atlantic exploiting a patchy environment . Ardea 87 : 177- Alcidae . Wilson Bull. 56 : 161-168 . 198 . Kuletz K.J. & Piatt J.F. 1999. Juvenile Marbled MurreCody M .L . 1971 . Ecological aspects of reproduction . let nurseries and the productivity index . Wilson In : Farner D .S . & King J .R. (eds) Avian Biology 1 : Bull. 111 : 257-261 . 462-512 Academic Press, New York . Lack D. 1968 . Ecological adaptations for breeding in Cramp S . (ed .) 1985 . The Birds of the Western Palearc- birds . Methuen & Co, London.

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Banner F.T., Collins M .B ., Massie K .S . (eds) The Ydenberg R.C. 1989 . Growth-mortality trade-offs and North-west European shelf seas: the sea bed and the the evolution of juvenile life histories in the Alcisea in motion II . Physical and chemical oceanograthe . Ecology 70 : 1494-1506 . phy, and physical resources: 467-493 . Elsevier Oceanography Series 24B, Elsevier, Amsterdam . Leopold M .F. 1991 . Toppredatoren op het Friese Front: SAMENVATTING zeevogels en zeezoogdieren. In : de Gee A, Baars M .A . & van der Veer H .W. (eds) De Ecologie van het Friese Front: 79-89. NIOZ Rapport 1991-2, De voedselvoorziening en de voor sterfte verantwoorNetherlands Institute for Sea Research, Texel . delijke factoren (waaronder het predatierisico) in de Lloyd C., Tasker M .L. & Partridge K . 1991 . The Status broedtijd worden wel beschouwd als de voornaamste of Seabirds in Britain and Ireland. T. & A.D . Poy- selectiemechanismen die hebben geleid tot een interser, London. mediaire uitvliegstrategie bij de Zeekoet Uria aalge . Mahoney S .P. & Threlfall W. 1981 . Notes on the eggs, Zeekoeten zijn semi-nestvlieders waarvan de jongen d e embryos and chick growth of Common Guillemots kolonie verlaten als kleine, gedeeltelijk bevederde kuiUria aalge in Newfoundland . Ibis 123 : 211-218 . kens op een leeftijd van ongeveer 20 dagen en met een McCanch N.V. 1981 . Predation on Manx Shearwaters lichaamsgewicht van ongeveer een kwart van dat van

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Monaghan P., Walton P., Wanless S ., Uttley J .D . & een adulte vogel. De jongen worden bij het verlaten van Burns M.D . 1994. Effects of prey abundance on the de kolonie vergezeld door een van beide ouders foraging behaviour, diving efficiency and time allo- meestal het mannetje - en van hun vertrek was tot voor cation of breeding gufflemots Uria aalge. Ibis 136 : kort niet veel meer bekend dan dat zij de zee opzwom214-222 . men. Toevallige waarnemingen in de centrale Noordzee Otto L., Zimmerman J.T.F., Fumes G .K ., Mork M ., en in kustwateren op grote afstand van de dichtstbijSa;tre R. & Becker G. 1990 . Review of the physical zijnde kolonies lieten zien dat de kuikens met hun begeoceanography of the North Sea . Neth. J. Sea. Res . leiders zich snel en tot een enorme afstand van de kolo26 : 161-238. nies verwijderen . De sterfterisico's voor kuikens die de Pearson T.H . 1968 . The feeding biology of sea-bird eerste `problematische' dagen na het uitkomen goed species breeding on the Fame Islands, Northumber. hebben doorstaan, zijn in de kolonie meestal laag . Na land. J. Anim . Ecol . 37 : 521-552 . Pingree R.D . & Griffiths D .K . 1978 Tidal fronts on the twee weken loopt de groei van de kuikens duidelijk shelf seas around the British Isles . J . Geoph . Res . terug doordat de oudervogels niet meer voorzien in de 83 C9 : 4615-4622 . snel toenemende voedselbehoefte van het zich ontwikSkov H., Durinck J ., Leopold M.F. & Tasker M.L . kelende jong. Van kuikens die de kolonie zojuist had1995 . Important bird areas for seabirds in the North den verlaten, kon echter worden vastgesteld dat de Sea, including the Channel and the Kattegat. Bird- groei op zee weer versnelde . Dit feit gaf aanleiding om life International, Cambridge. te denken dat de oudervogels niet in staat waren om Stearns S .C . 1992. The evolution of life histories . voldoende voedsel te brengen naar de kolonie . In dit Oxford Univ Press, Oxford . artikel wordt beschreven wat er gebeurt nadat de jonStone CJ ., Webb A., Barton C ., Ratcliffe N ., Reed T.C . ,

Tasker M .L ., Camphuysen C.J . & Pienkowski gen met de hen begeleidende oudervogel de kolonie M.W. 1995 . An atlas of seabird distribution in verlaten. Hiertoe werden tellingen van zeevogels op zee north-west European waters . Joint Nature Conser- voor de Schotse oostkust in de periode eind juni tot en vation Committee, Peterborough . met september geanalyseerd. Omdat voedsel kennelij k

Swennen C . 1977 . Laboratory research on seabirds . een beperkende factor is, al dan niet veroorzaakt door NIOZ-Report, Netherlands Institute for Sea het energetisch kostbare transport door de lucht (af- en Research, Texel . aanvliegende oudervogels van en naar verafgelege n Tasker M .L., Jones P.H., Dixon T.J . & Blake B .F. 1984 . foerageergebieden), werd verondersteld dat de ouderCounting seabirds at sea from ships : a review of vogels de jongen linea recta naar de dichtstbijzijnde methods employed and a suggestion for a standard- 'bekende . , voorspelbaar rijke en tot dan geëxploiteerde ' ized approach. Auk 101 : 567-577 . foerageergebieden zouden begeleiden . Tevens werd Tuck L .M . 1960. The Murres. Can. Wildl. Monogr. Ser . verondersteld dat de kleine kuikens om veiligheidsreNo . 1, Ottawa Weatherhead P.J . 1983 . Two principal strategies in denen, net als in de kolonie, naar gebieden zouden wor avian communal roosts. Am. Nat . 121 : 237-243 . den gebracht waar zij in grote groepen bescherming


tegen predatoren zouden kunnen vinden . Geen van bei- derden kilometers te maken op het moment dat de jonde veronderstellingen bleek het geval te zijn : de vol- gen nog kwetsbaar zijn en nauwelijks sterk genoeg lijwassen Zeekoeten begeleidden hun jongen naar de cen- ken om deze uitdaging aan te gaan . Immers, de overletrale Noordzee en verder. Zodoende passeerden ze de ving in de kolonie is na de eerste dagen zeer hoog en rijke foerageergebieden (herkenbaar aan de talloze weinig variabel, terwijl de overleving van jongen op actief foeragerende zeevogels, waaronder duizenden zee grote schommelingen vertoont . Vanuit het kuiken Zeekoeten zonder jongen, en dichte scholen vis) die redenerend zou een langer verblijf op de kolonie gunzich meestal op 50-100 km vanaf de kust bevonden . In stig zijn, zeker indien de volwassen vogels in staat zouplaats van zich in deze grote groepen te mengen, verko- den zijn om aan de toenemende voedselbehoefte van zen de `vader-kuikencombinaties' een reis in isolatie. het jong te voldoen . Dat laatste is niet onmogelijk, De groepsgrootte van jongen voerende Zeekoeten liep omdat in jaren van voedselschaarste uitgerekend Zeesnel terug bij toenemende afstand tot de kust om al snel koeten in staat blijken te zijn om door harder te werken op het minimum van één adulte vogel met één kuiken en verder te vliegen toch voldoende voedsel aan te voeuit te komen. Geconstateerd werd dat het predatierisico ren. Het niet tegemoetkomen aan de voedselbehoefte voor de kuikens in gebieden waar zich grote hoeveelhe- van het jong gedurende de laatste dagen voor het ùitden foeragerende zeevogels ophielden, groter zou kun- springen' is dan ook vermoedelijk een keuze, en niet nen zijn omdat Grote Jagers Stercorarius skua en Grote zozeer onvermogen . Jongen in gevangenschap zijn Mantelmeeuwen Larus marinus in dit gedeelte van de bovendien bij een onbeperkt voedselaanbod na drie Noordzee ongeveer tienmaal talrijker waren dan verder weken opvallend rusteloos en minder hongerig, een uit de kust. Kwantificering van voedselaanbod met indicatie dat het vertrek uit de kolonie `voorgeprogramakoestische signalen suggereerde echter dat dichte vis- meerd' is . Adulte vogels ondergaan na de broedtijd een scholen op de open Noordzee veel schaarser waren dan complete rui en zijn dan 40-45 dagen niet tot vliegen in in de foerageergebieden waar zich concentraties zeevo- staat . Succesvolle broedvogels keren al vroeg op de gels ophielden . De vertrekkende Zeekoeten verkozen kolonies terug om de beste broedrichels te verdedigen kennelijk een gebied met schaarste (zowel wat betreft voor het komende seizoen . Voor adulte vogels is de voedsel als wat betreft gevederde predatoren) boven tijdsdruk dus aanzienlijk . Het is mogelijk dat vroegtijeen gebied met overvloed . Veel van de `vader-kuiken- dig vertrek met jong bijdraagt aan de mogelijkheden combinaties' verlieten het onderzoeksgebied in het oos- om op tijd terug te keren, niet alleen voor de vogels die ten, op weg naar onbekende gebieden in de oostelijke `vrijaf' hebben (geen jong om te begeleiden), maar ook Noordzee (vermoedelijk Skagerrak en Kattegat) . Een voor adulte vogels die tijdens de zorg voor de jongen op deel trok echter in zuidoostelijke richting . Deze vogels zee ruien . Aangetoond kon worden dat adulte vogels bereikten tenslotte de frontale overgang tussen het hel- met een ùitspringend' jong een ruiachterstand hebben dere water van de Centrale Noordzee en het troebele in vergelijking met de overige Zeekoeten op zee, maar kustwater, een gebied bekend als het `Friese Front' . In dat die achterstand snel werd goedgemaakt tijdens het deze kennelijke `kraamkamer' was het voedselaanbod verzorgen van het jong op zee . rijk en voorspelbaar, terwijl de dichtheid aan potentiële predatoren hier tot oktober (wanneer de jonge Zeekoeten volgroeid zijn) laag was, vergelijkbaar met de situFirst received: 30 March 2000, re-submitted 20 Decematie op volle zee. ber 2001, accepted: 22 December 200 1 De vraag blijft waarom een relatief veilige omgeCorresponding editors : Theunis Piersma & ving (de kolonie) wordt verlaten om een reis van honRob G . Bijlsma