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TIMING AND SYNCHRONISATION OF BREEDING IN A MARSH TIT PARUS PALUSTRIS POPULATION FROM A PRIMAEVAL FOREST

TOMASZ WESOLOWSKI

Wesolowski T. 1998. Timing and synchronisation of breeding in a Marsh Tit Parus palustris population from a primaeval forest. Ardea 86: 89-100. Marsh Tits Parus palustris in Bialowieza National Park (E. Poland, 1985- 97) were single brooded, laid their first eggs between 5 April and 11 May (mean 21 April). Nest building commenced on average 10-15 days before the first egg was laid, but overlapped partially with egg laying. Median da­ tes of onset of laying in different years varied between 7 April and 26 April. Within a season laying was strongly synchronised as over 90% of birds commenced laying within ten days from the onset of the season. Early lay­ ing was correlated with high air temperatures. There were no differences in laying date between habitats. Females breeding for the first time on average laid two days later than in their following seasons. Otherwise, laying dates of individual females were repeatable between seasons. It is argued that the early and synchronised breeding of Marsh Tit is not so much an adaptation to the breeding season conditions but to a large extent a consequence of in­ tra-specific competition among young birds for a chance to settle, with ear­ ly fledged birds having strong competitive advantage. Key words: Parus palustris - Bilaowieza Forest - nest building - egg laying dates - weather conditions - nesting success - female age - repeatability Department of Avian Ecology, Wroc/aw University, Sienkiewicza 21, 50 335 Wroc/aw, Poland, E-mail: [email protected]

INTRODUCTION much less intensively studied. This stems prob­ ably from the fact that they are much less numer­ Organisms living in seasonal environments need ous than Great or Blue Tits, and only infrequently to breed at the most suitable period for succesful use nest-boxes. Except of a recent series of Swed­ reproduction. It is generally believed that this pe­ ish papers (Nilsson & Smith 1988ab; Smith riod should be timed such that the young are re­ 1993ab; Svensson 1995), there are only single pa­ ared during the most benign period (Daan et ai. pers (Dunn 1976; Schmidt 1984; Berndt & Winkel 1988). Both ultimate and proximate aspects of this 1987) in which the Marsh Tit breeding phenology question have been intensively studied in Great is reported. The existence of the last fragments of Tits Parus major and Blue Tits P. caeruieus. The­ primaeval, European lowland forest preserved se studies have revealed a whole array of factors within the strictly protected part of Bialowieza such as photoperiod, weather conditions, climate, National Park (E. Poland, hereafter referred to as food availability, habitat, predation, social status, BNP) has provided a unique opportunity to study adult age, body condition, genotype that can in­ the biology of birds in conditions free of direct fluence, with varying intensities, the onset of human disturbance (Wesolowski & Tomialoj6 breeding (Blondel et ai. 1990, 1993; Perrins 1996). 1995). Marsh Tits breed there at low densities, 1-2 Marsh Tits Parus paiustris, although breeding in territories 10 ha- 1 (Tomialoj6 & Wesolowski 1990, similar habitats as Great and Blue Tits, have been 1996), in natural holes (Wesolowski 1996a). Here I 90 ARDEA 86(1), 1998 describe variation in the laying dates of Marsh heights and contain a large amount ofdead timber Tits at different temporal (between- and within­ and uprooted trees (Tomialoj6 et al. (1984), Fa­ season) and spatial (local population, individual linski (1986), Tomialoj6 & Wesolowski (1990, bird) scales in relation to weather conditions, hab­ 1994). Oak-lime-hornbeam stands (Tilio-Carpine­ itat, nesting success, sex, age and genotype. Fi­ tum, 44.4% of the BNP strict reserve) are most nally, the possible selective pressures shaping the structurally diverse. They are composed of a doz­ timing of the Marsh Tit breeding period are dis­ en or so species of trees (mainly Hornbeam Car­ cussed, as well as the proximate mechanisms pinus betulus, Small-leaved Lime TWa cordata, which could be responsible for adjustment of on­ Pedunculate Oak Quercus robur, Norway Spruce set of breeding to varying environmental condi­ Picea abies, Norway Maple Acer platanoides), tions. that vary greatly with regard to age and size. In several stands the canopy is formed by trees over 200 years old, and often exceeding 250-400 STUDY AREA years. The amount of dead wood is intermediate between that found in the swampy and coniferous The Bialowieza Forest complex is situated on the stands. Swampy deciduous stands (Circaeo-Alne­ Polish-Belarussian border, the western part (580 tum, Carici elongate-Alnetum, jointly 21.6% of km2, ca. 45% of the area) being in Poland. The the reserve area) are more uniform, with the cano­ Forest represents a remnant of the vast lowland py composed mostly of Alder Alnus glutinosa, forests that once covered large parts of temperate Ash Fraxinus excelsior and Norway Spruce. This Europe. Its present unique features result from its habitat type is characterised by the largest amount considerable size and a good conservation status of dead wood: there are about three times more (Falinski 1986; Tomialoj6 et al. 1984; Tomialoj6 & fallen logs there than are in the oak-hornbeam Wesolowski 1990; Wesolowski & Tomialoj6 1995). stands (Wesolowski 1983). The coniferous stands Though traces ofhuman presence are known from (28.1 % of area) are usually not inhabited by the Neolithic period, intensive timber cutting did Marsh Tits. not start before the beginning of this century. The majority of tree stands in the Polish part are now under management, but a block of the best pre­ METHODS served primaeval stands has been strictly protect­ ed within BNP. Data on Marsh Tit nesting were collected with The primaeval stands in the strict reserve of varying intensity during 1979-1997. Intensive BNP are distinguished by a whole array of fea­ searches for nests, aimed at finding the holes of tures. They are multi-storey, mixed-species, un­ all breeding pairs, were made in four deciduous even-aged, composed of trees reaching unusual areas (plots K, C, M, and W) in 1987-89 and

Table 1. Study plots and forest types, including plot size (ha), main tree stands (%% after Wesolowski 1996a), and corresponding plot coding (Tom) as used by Tomialoje et at. (1984).

Plot size forest type main tree stands Tom.

K 33 ha riverine forest Ash,Alder K at forest edge C 48 ha forest interior S.-1. Lime (46%), Hornbeam (24%), N. Spruce (23%) CW,CE M 54 ha forest interior Hornbeam (47%), SA. Lime (27%), N. Spruce (13%) MS,MN W 50ha forest edge Hornbeam (34%), SA. Lime (28%), N. Spruce (18%) WE, WI Wesolowski: TIMING OF BREEDING IN MARSH TITS 91

1992-1997 (Table 1). The plots were 1-6 km son. This allowed us to compare individual birds apart. In other years nestholes were found mainly in consecutive seasons. After their first breeding during bird censuses carried out in the same four attempt, Marsh Tits are extremely sedentary, al­ plots (Tomialojc et af. 1984; Tomialoje & We­ most always staying in the same range for the rest solowski 1994, 1996). To determine breeding and of their life (T. Wesolowski, unpubl. data). Thus, nesting success, cavities were regularly checked, uminged birds settling in areas previously used mostly from the ground. Around the expected by ringed ones, are probably mostly young birds fledging date, they were inspected every 24 hrs. breeding for the first time. We therefore treated The day following the last day in which feeding uminged birds as young, first-time breeders. With of young in a hole was observed was taken as the this approach some older birds which had escaped fledging date. First egg dates were seldom direct­ catching in previous years will have been treated ly recorded in the field since, despite efforts to as first-time breeders. Note that the category of find nests at the building stage, numerous nests older birds is not so biased, as it contains only co­ were found only later. Moreover, even when a lour-ringed birds breeding for at least their second nest was found early enough, it was difficult to as­ time. certain whether laying already had commenced: Data on leaf-eating caterpillars, constituting nest cups were filled with wool around the laying an important source of nestling food, were col­ period and it was often not possible to see if they lected in May, the timing depending on the stage contained eggs. Therefore, it was necessary to of leaf development. Each time 50-120 standard back-calculate the first egg dates. To do this, it twigs (0.25 m2) from the lower parts of the horn­ was assumed that one egg is laid per day, that in­ beam undercanopy were searched and the cater­ cubation lasts 15 days, and that nestling age cor­ pillars counted. Original values of the caterpillar responds roughly to the stages given in Winkel index are given in Wesolowski & Tomialojc (1970) for Blue Tit. When clutch size and/or nest­ (1997). Meteorological data are from the local ling age were unknown (e.g. in holes observed weather station in Bialowieza village, situated in only from a distance or in holes containing only a the centre of Bialowieza Forest complex, less than single nestling), 40 days were subtracted from the 1 km from the southern edge of BNP (Wesolow­ fledging date. This comprised six days allowed ski and Stawarczyk 1991). To investigate the influ­ for egg-laying (a 7 egg clutch was assumed), 15 ence of spring temperatures on laying dates, fol­ days for incubation and 19 days for the nestling lowing Orell & Ojanen (1983), Schmidt (1984) stage (T. Wesolowski unpubl. data). and Perrins & McCleery (1989), sums of mean First egg dates were calculated as absolute daily temperatures >O°C (,warmth-sums', WS) (calendar) dates expressed as the number of days for three periods (30, 45 and 60 days) ending on since 1 April. Relative dates were calculated as the same fixed date were calculated. The fixed da­ the deviations in number of days of individual te was set at 16 April, i.e. five days before the av­ laying dates from the median absolute laying da­ erage date of laying in the population, coinciding tes (set 0) of respective years. Relative dates were with the period of rapid follicle growth and final calculated only for seasons with large samples of production of the egg (Kluyver 1952). The days nests. Three very late nesting attempts, com­ with above zero temperatures in the analysed ma­ menced long after the majority of birds were ex­ terial were concentrated within the last 30 days cluded from this analysis, as they could have been period. Hence, WS calculated over longer periods replacements (confirmed for the outlier in 1995). were redundant and could not be treated as inde­ Adults carrying food for nestlings were caught in pendent data points. Therefore, only WS for the door-traps placed at the hole entrance, and colour­ 30 days period are presented. Statistical analyses ringed. The majority of birds (up to 90% of birds were made using the Statistica software package in some years) were ringed by the end of the sea- (Anonymous 1996). 92 ARDEA 86(1), 1998

Table 2. Median laying dates of Marsh Tits, nest losses (n and %) and abundance of leaf-eating caterpillars at BNP in different years

Year Median Nest losses Caterp. twig- 1 (April) n %

1987 26 23 17.4 0.2 1988 19 26 15.4 1.0 1989 15 33 15.2 1.9 1992 16 34 11.8 24.9 1993 22 33 6.1 44.2 1994 19 42 16.7 7.4 1995 22 37 13.5 9.1 1996 25 33 27.3 0.6 1997 26 38 28.9 0.8

RESULTS bringing moss on 31 March 1990, are the earliest records of Marsh Tits carrying nest material at Pre-laying period BNP. Allowing for the time needed to reach this Marsh Tits used only pre-existing cavities, al­ stage of nest construction (Fig. 1), nest building though they could enlarge them by removal of by some birds that year may have begun no later mould and debris (Wesolowski 1996a). As females than 26 March. sometimes abandoned cleaned cavities and built Several breaks between the end of building their nests in a second or even third cleaned hole, and laying were observed. Completed nests (nest this phase is treated as a part of nest site selection, cups filled with wool) stayed empty for 1-4 days and is referred to as the cleaning stage (Fig. 1). (mean 2.0, n = 7) in 1993, for 1-6 days (mean 3.5, Genuine nest building was divided in three phas­ n = 12) in 1994, and for 1-4 days (mean 2.3, n = es, according to the type of nest material brought 12) in 1996, with differences among years being by birds. Initially, (1) birds collected green moss statistically significant (ANOVA, F2,28 =3.74, P < to form a nest foundation, then (2) long hair to 0.04). These breaks were dependent on year, ex­ line the nest cup, and finally (3) wool to fill the cluding two outliers (10 and 12 days respective­ cup. Figure 1 shows the number of days between ly), which might have been due to physiological a bird performing each activity and the start of disorders (Wesolowski 1996b). laying. The minimum amount of time necessary for nest building in Marsh Tit was 4-5 days, with Egg-laying: variation between seasons the median between 10 and 15 days. The start of egg-laying varied between 5 April Earliest hole cleaning (23 March 1997) pre­ (1990) and 11 May (1979), a difference between ceded the onset of laying in that hole by 34 days. years of 37 days. In 66.3% of 330 cases, laying Cleaning and moss carrying ended before egg­ began between 16 April and 25 April, i.e. within a laying begun (except for two cases). There was lO-day period. Laying was initiated on average on extensive overlap between hair- and especially 21 April. Second broods were not recorded. There wool-bringing and egg-laying: the birds contin­ was a large variation in laying dates among sea­ ued to bring in lining material almost until the last sons (Fig. 2). Median dates differed significantly egg was laid and they covered the clutch with (ANOVA, FlO 313 =71.39, P < 0.001) an there was wool and hair before incubation started. A bird a 19 day diff~rence between the earliest (7 April bringing hair on 30 March 1990, and another 1990) and latest (26 April 1987 and 1997) years. Wesolowski: TIMING OF BREEDING IN MARSH TITS 93

240 wool (15) 90• 89 200 • hair (26) ~ 94 85 E 160 • • ::::l 92• moss (35) (/) -5 120 E 88• 87 ~ • clean (36) ;: 80 95•

• 97• -35 -30 -25 -20 -15 -10 -5 0 5 10 40 96 days from start laying 6 10 14 18 22 26 median laying date (April) Fig. 1. Timing of nest building phases in relation to date of egg-laying commencement. The values should Fig. 3. Median laying date in different years in rela­ be treated as minima, because each stage could actually tion to 'warmth-sums' (WS, see text) of the 30 day pe­ start earlier than recorded. Median values (dots), 25­ riod preceding 16 April. 75% values (boxes) and ranges (whiskers) are shown. Sample sizes in parentheses.

in late seasons (rs = 0.60, n = 9, P = 0.09; Table year (n) 2). There was a strong negative correlation be­ 1997 (41) tween spring temperatures (WS, see methods) 1996 (36) and median laying date (rn = -0.89, P < 0.001). In 1995 (36) conclusion, Marsh Tits laid significantly earlier in 1994 (43) warm springs (Fig. 3). 1993 (33) 1992 (33) Egg-laying: variation within season Within seasons, breeding was highly syn­ 1990 (12) chronised. The tits commenced laying within 8­ 1989 (33) 14 (mean 10.5) days, 75% of females laid eggs 1988 (26) 1987 (23) within a week, >90% within ten days (Fig. 4). Distribution of relative laying dates deviated from 2 1985 (8) normal (Goodness of Fit, X n = 25.01, P = 0.009); laying dates were concentrated in the first 5 10 15 20 25 30 35 part of the season. This synchronisation in the on­ days from April 1 set of laying suggests that birds attempted to lay Fig. 2. Distribution of laying dates at BNP in relation eggs as early as possible after the onset of favour­ to year. Medians (dots), 25-75% ranges (boxes), maxi­ able conditions. So, laying should be more syn­ mum and minimum values (whiskers) and outliers chronised in late than early springs. Indeed, it (small dots) are shown. took fewer days for the first 75% of females to commence laying in later than in early seasons but the correlation was not significant (r = -0.53, n There was no overlap of laying periods in early =9 years with nest samples >20, P =0.14). and late seasons (Fig. 2). There was a tendency Mean relative laying dates in four plots did towards later breeding in years with lower abun­ not differ significantly (ANOVA, F3•31O =0.27, P dance of leaf-eating caterpillars (rs =-0.56, n =9, =0.84) and differed by no more than half a day (­ P = 0.12) and towards increase of nesting losses 0.2-0.1). The chance of nest failure was not 94 ARDEA 86(1), 1998

16 en 4 >- til 14 ~ c 2 til 12 '0 Q) E ~ 10 0 til E g 8 .g o c ~ 0 -2 6 "iii "> 4 Q) "0 -4 2 male: young (196) old (38) young (31) old (56) o female: young old ~ 4 ~ 0 2 4 6 deviation from median date (days) Fig. 5. Mean relative laying dates in relation to age of parents. Whiskers mark ± standard deviation. Sample Fig. 4. Percentage distribution ofrelative laying dates sizes in parentheses. (day 0 is median date of a season). Data from eleven years pooled, outliers (see Fig. 2) not included. Solid line shows frequencies expected assuming normal dis­ tribution. young females, such that non-surviving young fe­ males had had a later laying date (mean ± SD, 1.0 ± 11.65, n = 57) than those which survived to strongly dependent on its relative laying date. Al­ breed in successive seasons (0.2 ± 7.41, n = 46). though the mean (± SD) date of onset of laying This difference was not significant, however (t­ was slightly earlier in successful (0.0 ± 2.91, n = test, two tailed; t = 1.20, P =0.23). The surviving 253) than in failed nests (0.4 ± 2.44, n = 53), the females laid earlier in their second (mean ± SD, ­ difference was not significant (ANOYA, F 1,304 = 1.0 ± 5.23, n = 42) and third (-1.9 ± 8.20, n = 20) 0.36, P =0.36). breeding seasons. The difference between the first Young and old birds showed large scatter of two seasons (paired t-test, one tailed; t =3.64, P = laying dates (Fig. 4). However, pairs with young 0.001), but not between the latter two (t = 1.04, P females commenced laying about two days later = 0.16), was significant. Onset oflaying by the sa­ than pairs with older ones (MANOYA, F 1320 = me birds in consecutive seasons did not show any 22.47, P < 0.001). Neither age of male (MANO­ consistent pattern in males (repeatability = 0.07).

YA, F1,320 = 0.28, P = 0.60), nor interaction of Females, however, showed a significant tendency • partners' age (MANOYA, F1 320 = 0.49, P = 0.48) to breed at similar relative dates in successive contributed to this variation. The difference be­ years (r =0.23; Table 3). tween the female age classes could be partially at­ tributed to lower mortality of earlier breeding

Table 3. Repeatability of Marsh Tit relative laying dates in relation to sex. Repeatability calculated according to formula given by Lessels & Boag (1987).

Sex Effect Error F p r MS df MS df

Male 8.74 56 7.29 89 1.20 0.219 0.072 Female 12.13 45 6.60 84 1.84 0.008 0.229 Wesolowski: TIMING OF BREEDING IN MARSH TITS 95

DISCUSSION that sometimes birds may start to build too early for egg laying. The reverse situation, a delay in Data on timing of breeding gathered in primaeval egg-laying due to too a late start of nest construc­ conditions are free of several possible sources of tion could also occur, but is more difficult to dem­ bias that could affect results from man-trans­ onstrate. Building a nest, particularly the cleaning formed areas. Marsh Tits at BNP as they have al­ and enlargement of the nest hole, is time and en­ ways done, rely on diversified natural food (We­ ergy consuming, so these activities could interfere solowski 1995a), have to cope with a varied fauna with time needed to collect extra food to produce of predators (Wesolowski & Tomialoj6 1995), eggs. The building period in Bialowieza (10-15 breed at low densities (1-2 territories 10 ha- 1; To­ days) is twice longer than reported by other au­ mialoj6 & Wesolowski 1990, 1996) in natural holes thors (5-8 days; Steinfatt 1938; Morley 1953; (Wesolowski 1996a). In contrast, in man-trans­ Glutz von Blotzheim 1964; Markovets & Visotsky formed fragmented woods, the predator fauna is 1993), but these studies probably did not include usually impoverished, food of anthropogenic ori­ the hole cleaning stage in their figures. gin is frequently accessible, and densities of nest In birds living in highly seasonal environ­ box breeding tits are high (Wesolowski 1983; We­ ments, photoresponsiveness constitutes the basic solowski et af. 1987). It is impossible to say what mechanism setting the limits of the period in is the net effect of those differences on timing of which reproduction can occur (Immelmann 1971; breeding, since some, such as availability of addi­ Murton & Westwood 1977; Lambrechts et af. tional food or well insulated nest boxes may make 1996). Experiments by Clayton & Cristol (1996) earlier breeding possible (Kiillander 1974; O'Con­ on the impact of changes in day-length on food nor 1978), whereas other, like lowered numbers of storing behaviour in Marsh Tits may suggest that predators, can relax pressure on breeding early their yearly cycle is under strong photoperiodic (see below). The important point is that the selec­ control. tive pressures acting on birds in these two sets of Increasing day-length was probably the first conditions are very different, so that attempting to cue for birds preparing to breed. The observations answer ultimate questions using only data from of nest cleaning in the third decade of March in secondary woods, without reference to the histor­ 1990 occurred at day lengths as short as 11 hours. ical context (primaeval situation), can produce The birds at BNP must thus be physiologically misleading results. capable of breeding as early as birds from south­ ern populations - the average dates of onset of Timing of breeding - proximate control laying in northern Italy were 30 March - 18 April, The nest-building stage is usually ignored in with 8 April as a multi-year mean (Minelli et af. considerations of timing of breeding. This is 1995). This potential is however only rarely real­ probably a consequence of the fact that first egg ised, since in the majority of years breeding oc­ date, as the easiest variable to measure accurately curred on much later dates. The strong negative in the field, is most often used to measure the date correlations with warmth-sums recorded also in of commencement of breeding. However, birds Germany (Schmidt 1984) suggest that, as in other cannot skip this stage, as the start of nest con­ tits (Kluyver 1952; Perrins 1965; Van Balen 1973; struction must precede the start of egg-laying. Orell & Ojanen 1983; Nager 1990), onset oflaying Observations at BNP show that these phases can was directly or indirectly influenced by spring be separated by over a month. The occurrence of temperatures. However, if temperatures acted di­ pauses of variable length between end of nest rectly, then their thresholds of acceptance were construction and the start of egg-laying, especial­ not fixed. Much higher daily temperatures were ly pronounced in 1994, when birds with ready necessary to induce breeding early than late in the nests postponed laying for several days, suggests season. This implying that there was a link be- 96 ARDEA 86(1), 1998 tween temperature and the calendar date or day with the short yearly peak of availability of defol­ length to trigger commencement of breeding. iating caterpillars (Perrins 1965; Van Balen 1973; Marsh Tits may also respond proximately to some Zandt et at. 1990; Dias & BlondeI1996). Caterpil­ correlate of increasing temperatures, e.g. increas­ lars also constitute important ingredient of Marsh ing amount of food (Perrins 1970). If food is of Tit nestling food (Cramp & Perrins 1993; Glutz primary importance, a spatial variation in onset of von Blotzheim & Bauer 1993; T. Wesotowski un­ breeding related to variation in proportion of tree publ. data), but Marsh Tits start breeding earlier species, and phenology of vegetation develop­ than the other species (Dunn 1976; Schmidt 1984; ment in different habitats would be expected. The Berndt & Winkel 1987; Nilsson & Smith 1988a; study plots at BNP differed vastly in those re­ Minelli et at. 1995), so their young will hatch be­ spects (Faliflski 1986; Wesotowski 1996a), but the fore the peak availability ofcaterpillars. Hence, in distribution of laying dates did not vary among Marsh Tits the post-fledging rather than the nest­ them. By provisioning Marsh Tits with food in the ling period coincides with the peak availability of pre-laying period, Svensson (1995) could advance caterpillars. egg-laying by three days, a rather modest increase Avoidance of competition for holes or food in comparison with the huge variation of laying (Minot 1981; Nilsson 1984, 1986) with later breed­ dates observed in BNP among years. Both these ing dominant species could select for early breed­ results indicate that availability of food, though ing, but there is little support for this from the not without influence, can not be the sole cue used Biatowieza studies. Conflicts over holes do occur, by birds to decide when to reproduce. but their effect on numbers and distribution of Whatever the nature of environmental sig­ birds seem negligible. Holes are superabundant nal(s) triggering reproduction, it seems that it is and many ofthem remain unutilised. Even the lat­ perceived the same way by the majority of birds. est breeding birds such as flycatchers Ficeduta As in a Swedish study (Smith 1993b), young fe­ spp. in years of highest density do not face a male March Tits commenced laying about two shortage of holes (Wesotowski 1989; Walankie­ days later than older birds. There is, however, a wicz 1991; Mitrus et at. 1996). Foliofagous cater­ substantial dissimilarity in mechanisms which pillars are abundant in most years (Wesotowski & were responsible for bringing about those age-de­ Tomiatoj6 1995, 1997), so there may be little com­ pendent variation in relative laying dates. Smith's petition for food. (1993b) results gave some support to Curio's At BNP, nest predation pressure increases (1983) 'poor quality birds' hypothesis, i.e. selec­ within a season (Wesotowski 1985; Piotrowska & tive mortality of late-laying females. In this study, Wesotowski 1989). So, it would be advantageous the main mechanism of change appeared to be to breed early to avoid nest robbing. Marsh Tits phenotypic as the same females laid on average had the lowest nest-losses of all species so far about two days earlier when breeding for the sec­ studied in Biatowieza (Walankiewicz 1991; We­ ond time. Therefore, their later breeding in the sotowski & Stawarczyk 1991; Wesotowski & To­ first season could be due either to constraint, the miatoj6 1995; Wesotowski 1995b). That early inability to commence laying earlier by inexperi­ breeding might contribute is suggested by the enced birds, or to restraint, the inhibition of the finding that nest losses were higher in late first-time breeders from investing too heavy in springs. their first nesting attempt. The timing of breeding may not be optimised, because it depends on the timing of other events Timing of breeding - ultimate aspects in the yearly cycle. Nilsson & Smith (1988a) and The breeding season of Great and Blue Tits, Nilsson (1989) demonstrated that dispersal and that feed their young with leaf-eating caterpillars, establishment phases in Marsh Tits are very brief: is adjusted so that their nestling period coincides young birds attempt to establish themselves only Wesolowski: TIMING OF BREEDING IN MARSH TITS 97 a few days after family break-up. Their chance of ta from S. Sweden. The remarks ofW. Kania, P. Chyla­ establishment is strongly negatively correlated recki and two anonymous referees on an earlier draft of with relative fledging date, and a delay of even the paper are also acknowledged. few days being important. Thus, to enhance com­ petitive abilities of young and their chance of es­ tablishment, parents should start breeding as early REFERENCES as possible. Such a selection pressure could ex­ Anonymous 1996. Statistica for Windows. StatSoft, plain why Marsh Tits, in spite of laying earlier Inc., Tulsa. than Great and Blue Tits, hardly produce any sec­ Berndt R. & W. Winkel 1987. Bestandsentwicklung ond broods (Nilsson & Smith 1988a). It could be und Brutzeit-Daten der Sumpfmeise (parus palus­ also responsible for the highly synchronous breed­ tris): befunde aus dem siidostlichen Niedersachsen. ing recorded not only at BNP, but also in southern Vogelwelt 108: 121-131. Blondel J., PC. Dias, M. Maistre & P. Perret 1993. Sweden (90% of up to 48 pairs commenced laying Habitat heterogeneity and life-history variation of within 7-9 days; I-A. Nilsson pers. comm.), and in Mediterranean Blue Tits (Parus caeruleus). Auk Russia (70% of 64 nests hatched within a five-day 110: 511-520. period; Markovets & Visotsky 1993). Blondel J., P. Perret & C.M. Maistre 1990. On the ge­ With the pressure to breed early some adapta­ netic basis of the laying date in an island population of Blue Tits. J. Evo!. Bio!. 3: 469-475. tions to lessen costs of breeding early may have Clayton N.S. & D.A. Cristol 1996. Effects of photope­ developed. Feeding of egg-laying and incubating riod on memory and food storing in captive marsh females by males (Steinfatt 1938; Morley 1949; tits, Parus palustris. Anim. Behav. 52: 715-726. Nilsson & Smith 1988b) enable females to cover Cramp S. & e.M. Perrins (eds) 1993. The birds of the energy needs in shorter time. As this habit is not Western Palearctic. Vo!. 7. Oxford Univ. Press, Ox­ ford. unique to Marsh Tit, it remains to be shown that Curio E. 1983. Why do young birds reproduce less Marsh Tit males cover larger proportion of fe­ well? Ibis 125: 400-404. males energy requirements than males of later Dias P.e. & J. Blonde!. 1996. Breeding time, food sup­ breeding tits (Royama 1966; Krebs 1970). One ply and fitness components of Blue Tits Parus cae­ may predict that some additional mechanisms are ruleus in Mediterranean habitats. Ibis 138: 644­ 649. likely to be found as well. Measuring insulating Daan S., C. Dijkstra, R. Drent & T. Meijer. 1988. Food properties of holes and nests or a thorough study supply and the annual timing of avian reproduction. of female and embryo metabolism seem reward­ Proc. intern. am. Congr XIX: 392-407. ing avenues for further research. Dunn E. 1976. Laying dates of four species of tits in Wytham Wood, Oxfordshire. Brit. Birds 69: 45-50. Falmski J.B. 1986. Vegetation dynamics in temperate forests (Ecological studies in Bialowieza Forest). ACKNOWLEDGEMENTS Junk Pub!., Dordrecht. Glutz von Blotzheim U.N. 1964. Die Brutvogel der I heartily thank T. Klis, K. Konieczny, J. Lontkowski, Schweiz. Aarauer Tagblatt, Aarau. C. Mitrus, J. Nowakowski, 1. Oleksik, B. Orlowska, Glutz von Blotzheim U.N. & K.M. Bauer 1993. Hand­ P. Rowmski, T. Stawarczyk, A. Szymura, 1.. Tomialojc, buch der Vogel Mitteleuropas. Vo!. 13. Akademis­ W. Walankiewicz, and J. Wroblewski for their partici­ che Verlagsgesllschaft, Wiesbaden. pation in the field work. The financial aid of the Eco­ Immelmann K. 1971. Ecological aspects ofperiodic re­ production. In: Farner D.S. & J.R. King (eds) Avian logical Institute and the Zoological Institute of the Po­ biology, 1: 342-389. Academic Press, New York. lish Academy of Sciences, as well as that of ALA, Kallander H. 1974. Advancement of laying of Great Schweizerische Vogelwarte, the Ministry of Environ­ Tits by the provision of food. Ibis 116: 365-367. mental Protection & Natural Resources and National Kluyver H.N. 1952. Notes on body weight and time of Fund For Environment Protection and Water Manage­ breeding in the Great tit (Parus major). Ardea 40: ment, helped to cover costs of field work in various pe­ 123-141. riods. J-A. Nilsson kindly provided his unpublished da- Krebs J. R. 1970. The efficiency of courtship feeding in 98 ARDEA 86(1), 1998

the Blue Tit, Parus caeruleus. Ibis 112: 108-110. Orell M. & M. Ojanen 1983. Timing and length of the Lambrechts M.M., P. Perret & J. Blondel. 1996. Adap­ breeding season of the Great Tit, Parus major, and tive differences in the timing of egg laying between the Willow Tit, P. montanus, near Ou1u, Northern different populations of birds result from variation Finland. Ardea 71: 183-198. in photoresponsiveness. Proc. R. Soc. London B Perrins C.M. 1965. Population fluctuations and clutch­ 263: 19-22. size in the Great Tit, Parus major L. J. Anim. Ecol. Markovets M.Yu & V.G. Visotsky 1993. [Breeding bi­ 34: 601-647. ology of the Marsh Tit (Parus palustris) on the Perrins C.M. 1970. The timing of birds' breeding sea­ Coursih Spit.] Rus. J. Omithol. 23: 61-69. (In Rus­ sons. Ibis 112: 242-255. sian, English summary) Perrins C.M. 1991. Tits and their caterpillar food sup­ Minelli E, G. Cerre & A. Spampanato 1995. Densita e ply. Ibis 133 suppl. 1: 49-54. bio1ogia riproduttiva di Cincia bigia Parus palustris Perrins C.M. 1996. Eggs, egg formation and the timing in uno bosco dell'Appennino bolognese. Picus 21: of breeding. Ibis 138: 2-15. 115-124. Perrins C.M. & R.H. McCleery 1989. Laying dates and Minot 1981. E. O. 1981. Effects ofinterspecific compe­ clutch size in the Great Tit. Wilson Bull. 101: 236­ tition for food in breeding blue and great tits. J. 253. Anim. Ecol. 50: 375-386. Piotrowska M. & T. Wesolowski 1989. The breeding Mitrus C., W. Walankiewicz, D. Czeszczewik & P.M. ecology and behaviour of the Chiffchaff Phyllosco­ Jablonski 1996. Age and arrival date of Collared pus collybita in primaeva1 and managed stands of Flycatcher Ficedula albicollis males do not influ­ Bialowieza Forest (Poland). Acta om. 25: 25-76. ence quality of natural cavities used. Acta om. 31: Royama T. 1966. A re-interpretation of courtship feed­ 101-106. ing. Bird Study13: 16-129. Morley A. 1949. Observations on courtship-feeding Schmidt K-H. 1984. Frtihjahrstemperaturen und Le­ and coition of the Marsh-Tit. Brit. Birds 42: 233­ gebeginn bei Meisen (Parus). J. f. Omithologie 239. 125: 321-331. Morley A. 1953. Field observations on the biology of Smith H.G. 1993a. Seasonal decline in clutch size of the Marsh Tit. Brit. Birds 46: 32-346. the Marsh Tit (Parus palustris) in relation to date­ Murton R.K. & N.J. Westwood 1977. Avian breeding specific survival of offspring. Auk 110: 889-899. cycles. Clarendon, Oxford. Smith H.G. 1993b. Parental age and reproduction in the Nager R.G. 1990. On the effects of small scale varia­ Marsh Tit Parus palustris. Ibis 135: 196-201. tion in temperature and food availability on laying Steinfatt O. 1938. Das Brutleben der Sumpfmeise und date and egg size in great tits (Parus major). In: einige Vergleiche mit dem Brutleben der anderen Blondel J., A. Gosler, J.D. Lebreton & R. McClee­ einheimischen Meisen. Beitr. Fortpfl. 14: 137-144. ry (eds) Population biology ofpasserine birds: 187­ Svensson E. 1995. Avian reproductive timing: when 197. Springer, Berlin. should parents be prudent? Anim. Behav. 49: 1569­ Nilsson J-A. 1989. Establishment ofjuvenile marsh tits 1575. in winter flocks: an experimental study. Anim. Be­ Tomialoj6 L. & T. Wesolowski 1990. Bird communities hav. 38: 586-596. of the primaeval temperate forest of Bialowieza, Nilsson J-A. & H.G. Smith 1988a. Effects of dispersal Poland. In: Keast A. (ed.). Biogeography and ecol­ date on winter flock establishment and social dom­ ogy offorest bird communities: 141-165. SPB Aca­ inance in Marsh Tits Parus palustris. J. Anim. Ecol. demic Publ. bv, The Hague. 57: 917-928. Tomialoj6 L. & T. Wesolowski 1994. Die Stabilitat der Nilsson J-A. & H.G. Smith 1988b. Incubation feeding Vogelgemeinschaft in einem Urwald der gemassig­ as a male tactic for early hatching. Anim. Behav. ten Zone: Ergebnisse einer 15jahrigen Studie aus 36: 641-647. dem Nationalpark von Bialowieza (Polen). Om. Nilsson S.G. 1984. The evolution of nest-site selection Beob. 91: 73-110. among hole-nesting birds: the importance of nest Tomialoj6 L. & T. Wesolowski 1996. Structure of a pri­ predation and competition. Omis Scand. 15: 167­ maeval forest bird community during 1970s and 175. 1990s (Bialowieza National Park, Poland). Acta Nilsson S.G. 1986. Evolution of hole-nesting in birds: om. 31: 133-154. on balancing selection pressures. Auk 103: 432­ Tomialoj6 L., T. Wesolowski & W. Walaukiewicz 1984. 435. Breeding bird community of a primaeval temperate O'Connor R.J. 1978. Nest-box insulation and the tim­ forest (Bialowie:i:a National Park, Poland). Acta ing of laying in the Wytham Woods population of om. 20: 241-310. Great Tits (Parus major). Ibis 120: 534-537. Van Balen J.H. 1973. A comparative study ofthe breed- Wesolowski: TIMING OF BREEDING IN MARSH TITS 99

ing ecology of the Great Tit in different habitats. SAMENVATTING Ardea 61: 1-93. Walankiewicz W. 1991. Do secondary-cavity nesting In dit artikel wordt de timing van het broeden van de birds suffer more from competition for cavities or Glanskop Parus palustris beschreven op grond van on­ from predation in a primaeval deciduous forest? derzoek in het 'oerwoud' van Bialowieza Nationaal Natural Areas J. 11: 203-212. Wesolowski T. 1983. The breeding ecology and behavi­ Park in het oosten van Polen. In deze grotendeels onge­ our of Wrens Troglodytes troglodytes under pri­ repte bossen werden over een periode van elf jaren ge­ maeval and secondary conditions. Ibis 125: 499­ gevens verzameld over nestbouw en eileg van de 515. Glanskop. De gevonden variaties (op ruimtelijke en Wesolowski T. 1985. The breeding ecology of the wood temporele schaal) werden in verband gebracht met warbler Phylloscopus sibilatrix in primaeval forest. weersomstandigheden en biotoop, maar ook met broed­ Omis Scand. 16: 49-60. succes, geslacht en leeftijd van de vogels. De onder­ Wesolowski T. 1989. Nest-sites of hole-nesters in a pri­ zochte Glanskoppen in de bossen van Bialowiei:a broe­ maeval temperate forest (Bialowieza National Park, den in natuurlijke holtes met een dichtheid van 1-2 pa­ Poland). Acta om. 25: 321-351. ren ha-!. Deze holtes werden vanaf eind maart bezocht, Wesolowski T. 1995a. Birds from a primaeval temper­ ate forest hardly use feeders in winter. Omis Fenn. waarbij de mezen allereerst de romrnel uit de holtes 72: 132-134. verwijderden (vroegste datum 23 maart 1997,34 dagen Wesolowski T. 1995b. Ecology and behaviour of Whi­ voordat in dat nest eieren werden gelegd). Vervolgens te-backed Woodpecker (Dendrocopos leucotos) in werd vanaf begin april nestmateriaal (haar, mos, wol) a primaeval temperate forest (Bialowieza National ingevlogen, waama met de eileg kon worden begonnen. Park, Poland). Vogelwarte 38: 61-75. Het begin van de eileg varieerde van 5 april (1990) tot Wesolowski T. 1996a. Natural nest sites of Marsh Tit 11 mei (1979), een periode van 37 dagen, met 66.3% Parus palustris in a primaeval forest (Bialowieza van 330 gevallen tussen 16 april en 25 april. De media­ National Park, Poland). Vogelwarte 38: 235-249. ne begindatum verschilde 19 dagen tussen de vroegste Wesolowski T. 1996b. [Incubation of empty nests and (1990, 7 april) en laatste seizoenen (1987 en 1997, 26 other incubation disorders in the Marsh Tits (Parus palustris) at Bialowiei:a National Park]. Notatki or­ april). Binnen de verschillende seizoenen was het begin nitol. 37: 148-151. (In Polish, English summary) van de eileg in hoge mate gesynchroniseerd (75% van Wesolowski T. & T. Stawarczyk 1991. Survival and aile wijfjes legden dezelfde week, gemiddeld aile bin­ population dynamics of Nuthatches Sitta europaea nen 10.5 dagen). In warme voorjaren begonnen de me­ breeding in natural cavities in a primaeval temper­ zen eerder met de eileg dan in koude voorjaren (media­ ate forest. Omis Scand. 22: 143-154. ne eileg versus 'warmte-som' (som van gemiddelde Wesolowski T. & L. Tomialojc. 1995. Omithologische dagtemperatuur over de voorgaande dertig dagen), r = ­ Untersuchungen im Urwald von Bialowieza - eine 0.89, P < 0.001, n = 11). Tussen de verschillende gebie­ Ubersicht. Om. Beob. 92: 111-146. den, elk met hun eigen vegetatie-type, bestond elk sei­ Wesolowski T. & L. Tomialojc. 1997. Breeding bird dy­ zoen maar weinig variatie in het begin van de eileg. namics in a primaeval temperate forest: Long-term trends in Bialowieza National Park (Poland) ­ Jonge wijfjes (eerste jaar) begonnen gemiddeld twee Ecography 20: 432-453. dagen later met de eileg dan meer ervaren broedvogels Wesolowski T., L. Tomialojc & T. Stawarczyk. 1987. (tweede jaar) onder dezelfde condities en broedvogels Why low numbers of Parus major in Bialowiei:a in die een derde weer werden aangetroffen konden nog Forest - removal experiments. Acta om. 23: 303­ weer eerder met broeden beginnen dan in de eerste 316. twee seizoenen. Winkel W. 1970. Hinweise zur Art- und Altersbestim­ Waar in veel studies de eileg als het begin van het mung von Nestlingen hohlenbrtitender Vogelarten broeden wordt aangemerkt maakt deze studie duidelijk anhand ihrer Korperentwicklung. Vogelwelt 91: 52­ dat er weI een maand kan zitten tussen de keuze van de 59. nestholte, het geschikt maken van het nest en de uitein­ Zandt H.S., A.M. Strijkstra, J. Blondel & J.H. van Balen. 1990. Two Mediterranean Blue Tit populations: are delijke eileg. Omdat de nestbouw (in elk geval onder differences in the timing of breeding associated with deze natuurlijke omstandigheden) een tijd- en energie­ caterpillar availability? In: Blondel J., A. Gosler, J.D. vretende activiteit is, zijn er allerlei belangrijke keuze­ Lebreton & R. McCleery (eds) Population biology of momenten aanwijsbaar. Een te late nestbouw maakt passerine birds: 145-155. Springer, Berlin. bijvoorbeeld dat er niet geprofiteerd kan worden van 100 ARDEA 86(1), 1998 eventuele gunstige omstandigheden voor de eileg en verschillen met de andere twee mezensoorten zijn dat het broeden. In het stuk wordt aannemelijk gemaakt dat Glanskoppen vrijwel geen tweede broedsels kennen en de daglichtperiode en de temperatuur van grotere in­ de exceptionele synchronisatie van de periode van eileg vloed zijn op de grote variaties in de aanvang van het (veel korter dan bij de meeste zangvogels). Veronder­ broeden dan bijvoorbeeld variaties in het voedselaan­ steld wordt dat de timing van het broeden bij de Glans­ bod. Vit de hoge mate van synchronisatie blijkt dat, wat kop niet als zodanig is geoptimaliseerd, maar onderge­ de precieze signalen ook zijn, alle mezen op dezelfde schikt is geraakt aan andere factoren. Het blijkt dat jon­ stimulus reageerden. Het broedseizoen van Koolmees ge Glanskoppen zich al snel na het opbreken van de fa­ Parus major en Pimpelmees P. caeruleus is zo afge­ milies proberen te vestigen en dat er een sterk negatief stemd, dat de jongen uit het ei kruipen op het moment verband bestaat tussen hun vestigingssucces en de uit­ dat rupsen hun maximale talrijkheid hebben bereikt. vliegdatum. De intra-specifieke competitie maakt dat Glanskoppen broeden aanzienlijk eerder, zodat de jon­ een enkele dagen later beginnende eileg leidt tot in ho­ gen uitkomen v66rdat de rupsen hun piekvoorkomens ge mate gereduceerde kansen op een geslaagde vesti­ kennen. Of het broedseizoen van de Glanskop is erop ging van de jongen. (CJC) afgestemd dat de jonge mezen uitvliegen op het mo­ ment dat rupsen op het talrijkst zijn, of er is een andere Received 10 March 1997, accepted 15 November 1997 selectieve component in het spel. Andere opmerkelijke Corresponding editor: Leo Zwarts