Differences in the breeding performance of great tits Parus major between a forest and an urban area: a long term study on first clutches

Abstract

The great tit Parus major inhabits various types of forests, yet it prefers deciduous forests. In the urbanized areas it is one of the commonest bird species, even where only isolated trees are present, which seems to be a relatively recent phenomenon. This paper presents results of a long-term study (2002–2015) of variation in reproductive performance (number of hatchlings, hatching success, number of fledglings, fledging success, breeding success and nest failure rate) in first clutches of two great tit populations nesting in two contrasting habitats: a mature deciduous forest and an urban parkland, in central Poland. This study shows a clear and sustained spatial pattern of variation where the forest population of great tits produced more hatchlings and fledglings per successful nests than the urban park site population. Breeding success and fledging success demonstrate a similar but slightly less obvious pattern, with higher values for the forest site than the urban parkland area occurring consistently in the vast majority of years. Also hatching success was generally slightly higher in the forest than in the urban park but did not show such a clear spatial pattern. Only the nest failure rate was higher in the forest than in the urban parkland. We suggest that caterpillar richness in the forest compared to the urban parkland is one of the key drivers of the observed differences in the breeding performance between the study habitats. We also found positive correlations between fledgling numbers and caterpillar abundance and between fledgling numbers and mean May temperatures in the forest, whereas neither breeding nor fledging success showed such correlations. In the urban parkland, fledgling numbers as well as fledging and breeding successes were positively correlated with mean May temperatures. The between-population variation we found probably reflects a more general difference between urban and forest populations of tits.

Keywords:

• Great tit
• breeding performance
• breeding success
• urban population
• forest population

Introduction

Life-history theory predicts that optimal reproductive strategies should vary across environments because organisms living in various conditions undergo functional constraints among life-history traits, resulting from limited resources that must be allocated among competing demands (Stearns 1992). Selection optimizes the allocation of resources to achieve the most advantageous balance of phenotypic traits under particular ecological conditions (Ricklefs 2000). Life-history theory explains the general features of life cycle, i.e., lifespan, growth rate, number of offspring and reproductive attempts, which are connected with constraining relationships among each other and specific environmental requirements. This classic theory has been recently supplemented by the pace-of-life syndrome hypothesis (POLS), which predicts coevolution of life-history strategy with a set of co-varying traits in physiology, metabolism and behavior shaped and favored by adaptive adjustment to specific environmental conditions (Ricklefs & Wikelski 2002; Réale et al. 2010). For example, according to this theory, species (or individuals within a population) on the slow end of the axis should be characterized by complex life-histories (e.g. high survival and lower reproduction output), physiological traits (e.g. lower metabolism) and behavioral traits (e.g. lower activity and shyness), whereas species or individuals on the fast end of the axis should demonstrate opposite characteristics (Réale et al. 2010). Nowadays, important modifications of life-history traits and fast eco-evolutionary processes could be noticed primarily in rapidly changing environments, such as those connected with urban development (Alberti 2015).

Urbanization is one of the major causes of natural habitat loss and fragmentation on the global scale, as it modifies extensively the natural landscapes, leading to rearrangement of habitats and fauna composition (McDonnell & Pickett 1990; Chamberlain et al. 2009). Habitat modification associated with urbanization creates new, often highly heterogeneous areas with novel combinations of challenges and sometimes also benefits for birds (Chace & Walsh 2006; Gil & Brumm 2013; Seress & Liker 2015). Advantages of urban habitats are mostly connected with additional and predictable food resources (Anderies et al. 2007; Kumar et al. 2019), high availability of nest sites (Reynolds et al. 2019) and, in some cases, with a reduced predation pressure (Vincze et al. 2017). Costs may be related to high human density and human disturbance (Fernández-Juricic & Tellería 2000), chemical pollution (Bichet et al. 2013), habitat fragmentation (Weldon & Haddad 2005). Numerous species suffer from these anthropogenic disturbances, which can cause changes in the diversity and abundance of an entire avian community by land transition from natural or semi-natural to urban, often driving biotic homogenization (see Chace & Walsh 2006; Marzluff 2016). Only a few species thrive in urban habitats, whilst many others sustain a mixture of advantages and costs of being urban inhabitants, whereas some species remain highly sensitive to stressors connected with environmental changes, the presence of people or have specific requirements and hence are absent or occur very rarely in urban areas (Fuller et al. 2009; Gil & Brumm 2013). In general, it has been suggested that species can be divided into three groups based on their levels of tolerance to urban disturbance – urban “avoiders”, “adapters” and “exploiters” (McKinney 2002). Species belonging to the “adapters” group are most interesting from the eco-evolutionary point of view because they make use of both natural and human-transformed habitats, and are thus very flexible in their lifestyles. These species evolved in natural conditions, yet rapid and drastic changes caused by urbanization force their specific adjustments, which are likely the result from phenotypic plasticity (Charmantier et al. 2017). The evolution of proper adaptations to novel conditions by natural selection on heritable variation may also be quite fast (Johnson & Munshi-South 2017). Recently, some authors have predicted that life-history traits should be formatted at the intraspecific level by particular urban ecology conditions, similarly to species communities, which are shaped by the specific ecological conditions of cities, preferring “urban-exploiter” species and eliminating sensitive species (Charmantier et al. 2017; Sprau et al. 2017; Sepp et al. 2018). It has been hypothesised that there exist adaptive differences in the pace of life (POLS) between urban and rural areas or even within the heterogeneous urban matrix (Sepp et al. 2018). It has been suggested that living in cities should lead to slower life histories (e.g. high survival, less investment in annual reproduction) in the pace-of-life continuum (from slow to fast), but in their behavioral features, urban birds should represent fast behavioral syndromes (e.g. boldness, high activity, high aggressiveness, more explorer behavior). On the other hand, the differences between urban and rural areas may also be attributed to variation in environmental conditions associated with urbanization, not necessarily as a manifestation of evolutionary adaptation, but instead, as a result of variation in food quantity and quality (Chamberlain et al. 2009). Alternatively, differences found between rural and urban populations, for instance reduction in the reproductive output, could be interpreted as consequences of the urban habitats being an ecological trap (Stracey & Robinson 2012; Sumasgutner et al. 2014).

Variation in reproductive performance is shaped by the interactions of extrinsic factors and intrinsic factors. Firstly, intrinsic factors connected with parental quality, age, health or experience have been proposed to explain such variation (Slagsvold & Lifjeld 1990; Gustafsson et al. 1994; Pärt 1995; Przybylo et al. 2001; Pagani-Núňez & Senar 2016; Caprio & Rolando 2017). Secondly, extrinsic factors, which are linked to differences in habitat quality (Martin 1987; Nager & Van Noordwijk 1992; Solonen 2001; Przybylo et al. 2001), food abundance (Cresswell & McCleery 2003; Massa et al. 2004; Marciniak et al. 2007), habitat structure and species composition of trees (Cowie & Hinsley 1987; Riddington & Gosler 1995; Mackenzie et al. 2014), home range size (Caprio & Rolando 2017), calcium abundance (Bańbura et al. 2010; Reynolds & Perrins 2010) or weather conditions (Massa et al. 2011; Bordjan & Tome 2014; Tobolka et al. 2015; Glądalski et al. 2016a) may also operate. Certainly, both types of factors influence bird reproductive success, but relations between them have often been confused.

Small urban passerines consistently exhibit earlier lay dates and smaller clutch sizes than their conspecifics in rural habitats (see reviews Chamberlain et al. 2009; Sepp et al. 2018). This is also true of great tits (Parus major) and blue tits (Cyanistes caeruleus) in our study system (Glądalski et al. 2015; Wawrzyniak et al. 2015). We have also shown that in both these tit species nestlings in the forest study area have on average better physiological condition than nestlings in the urban park area (Markowski et al. 2015; Kaliński et al. 2015a, 2015b, 2017a, 2017b; Glądalski et al. 2016b). Chamberlain et al. (2009), Marzluff (2016) and Sepp et al. (2018) have emphasized that further comparative research on differences in reproductive parameters between urban and non-urban populations of birds is needed.

The main effort of this study is focused on effects of such environmental factors as habitat type, year, caterpillar availability, weather conditions, and also – competition on variation in hatchling and fledgling numbers and corresponding success rates of great tits during 14 consecutive breeding seasons. Our predictions are: (1) forest and urban great tits should differ in the number of hatchlings and fledglings, so that forest birds should produce more hatchlings and fledglings as a result of higher clutch sizes, caterpillar abundance and a higher habitat quality; (2) hatching success and fledging success should be similar in both areas because clutch sizes are matched to local food resources or will be higher in the optimal natural environment in the forest (3) fledgling number and especially fledging success should be sensitive to trophic conditions, weather conditions and, perhaps, to great tit densities.

Material and Methods

Study areas

The present study was carried out in 2002–2015, around the city of Łódź, central Poland. Study areas are located about 10 km apart, in two contrasting types of habitats: an urban parkland and a rich deciduous forest. The urban parkland study site (51º45ʹN; 19º24ʹE), an area of ca. 80 ha (including the zoological garden of 16 ha and the botanical garden of 64 ha), has a highly fragmented tree cover. The total length of pathways per hectare is 4.5 times greater in the parkland than in the forest, and a mesh of paths is much denser in the parkland as well (Glądalski et al. 2016c). Both gardens are important recreation areas of the city of Łódź and they are visited by great numbers of people, especially in spring and summer. The vegetation of the Zoological Garden has been heavily fragmented and adapted to displaying animals. The vegetation of a large part the Botanic Garden has been planted artificially to exhibit plants, with extensive tree-free spaces. Dominant native tree species are pendulate oak (Quercus robur), sessile oak (Q. petrea), birches (Betula sp.), hornbeam (Carpinus betulus), scots pine (Pinus silvestris), poplars (Populus sp.), willows (Salix sp.), limes (Tilia sp.), maples (Acer sp.), and numerous exotic tree species.

The forest study site (51º50ʹN; 19º29ʹE) is ca. 130 ha area in the interior of a mature mixed deciduous forest (1250 ha in total), neighbouring with the NE suburbia of Łódź. Oaks Q. robur and Q. petraea are predominating species. In the surrounding of nest-boxes, these oaks constituted 51.2% of all trees, while coniferous species only 9%. In general, the density of trees in the surroundings of nest-boxes is about three times lower in the urban park site than in the forest site, while in the case of the native oaks the difference is even much higher (Glądalski et al. 2017). The tree age structure of the forest site is mostly mature, sometimes with trees over 100 years old and some dead trees being present.

Both study sites have been supplied with wooden nest-boxes with removable front walls. All nest-boxes were placed on trees (usually on oaks) at a height of 2.5–3 m. The number of nest-boxes generally increased over the study period with current numbers being c. 200 in the parkland area and c. 300 in the forest (see Glądalski et al. 2016d). We currently use two types of nest-boxes that differ in height (29 cm and 32 cm, respectively) and have similar floor dimensions, 11 cm X 11 cm. In the past, we used nest-boxes from different manufacturers that might slightly differ in these dimensions. In both study areas, distances between neighboring nest-boxes were about 50 m, and the density of nest-boxes did not differ between the two study areas (see Glądalski et al. 2016d). The nest-boxes in both study plots were also occupied by blue tit, less frequently by other bird species: pied flycatchers (Ficedula hypoleuca) and nuthatches (Sitta europea), and, occasionally, marsh tits (Poecile palustris) and coal tits (Periparus ater).

Data on caterpillar abundance

The abundance of caterpillars during the breeding seasons was measured indirectly, using the frass fall collecting method (Marciniak et al. 2007). The frass fall method allows to measure the amount of frass produced by caterpillars, which indicates caterpillar numbers and biomass available for tits (Zandt 1994). The abundance of caterpillars was monitored over the tit breeding seasons 2003–2015. Frass fall was collected into 1 m x 1 m tissue traps, hung below tree canopies, 9 in the forest and 5 in the parkland. The traps were checked and emptied every 5 days. In the laboratory, all of the gathered samples were inspected under a microscope to separate caterpillar frass from other particles, dried and weighed to the nearest 0.1 mg. The resulting masses were established for both study plots in a given year (for details see Marciniak et al. 2007). The peak caterpillar amounts differed significantly between the two study areas (Glądalski et al. 2017). According to Glądalski et al. (2017), the peak caterpillar abundance, as measured by the maximum amount of frass fall, averaged 0.21 ± 0.11 g frass/m²/day (range: 0.05–0.41) in the urban parkland and 0.59 ± 0.50 g frass/m²/day (range: 0.07–2.13) in the forest in 2003–2015. The peak amount of caterpillar frass in a season was used as a simple indicator of trophic richness in caterpillars, the fundamental food for chicks (Cholewa & Wesołowski 2011).

Breeding density data

Great tit (and also blue tit) nest-box breeding density data (including seasons 2002–2012) were subject of our previous analyses, and in all study years we recorded that at least 20% of nest-boxes were not occupied by any species of bird, so we concluded that availability of nest-boxes was not a limiting factor for numbers of breeding pairs (see Glądalski et al. 2016c). We used breeding density data (2002–2015) as one of the potentially important factors that can have an impact on the breeding performance. The evaluation of the density of great tits was based solely on breeding pairs nesting in nestboxes; the numbers may be underestimated, especially in the forest site, because of the presence of many natural holes, sometimes occupied by tits (own observations).

Data on weather conditions

We took into account also weather conditions in years 2002–2015. Mean hatching dates in both study sites took place in May, therefore, the nestling rearing stage in all years occurred in that month in the case of most breeding pairs. Because weather conditions in May have an important role in nestling survival until leaving the nest, we decided to focus attention on this month. The local temperatures for Łódź were obtained from the TuTiempo.net climate database for Łódź (http://www.tutiempo.net/en/Climate/LODZ/124650.htm and https://en.tutiempo.net/climate/ws-121055.html).To characterize weather conditions in May we use two measures: mean temperature and total rainfall (sum of rainfall) (Figure 1)

Figure 1. Mean May temperature (^oC) and May rainfall sum (mm) in study period 2002–2015 in Lodz.

Great tit breeding data

During the breeding season, the study sites were visited daily to record nest-box occupancy, laying date, clutch size, the number of hatchlings and the number of fledglings. We calculated hatching success as the number of hatchlings in relation to clutch size, and fledging success as the number of fledglings in relation to the number of hatchlings (refers to the nests from which at least one young fledged). Breeding success was calculated as the number of fledglings in relation to clutch size.

During 2002–2015, we collected information about 1275 complete first clutches (meaning clutches that were incubated). For years when any experiments were carried out, we took into consideration only clutches which were not subjected to experimental treatments (Table I). In the analysis, we generally focus on successful nests, whereas data on completely failed nests we only presented descriptively. Analyses of fledgling numbers in relation to years and study sites refer to the nests from which at least one young fledged, and therefore we took into account 1078 broods (628 in the parkland and 450 in the forest). We determined an exact number of hatched chicks in 976 successful broods and 103 failed broods, so analyses of hatchling numbers and hatching success were conducted on 1079 nests (616 in the parkland and 463 in the forest), while analyses of fledging success on 976 nests (569 in the parkland and 407 in the forest) for which we had accurate data on hatchling numbers.

Table I. The numbers of complete clutches and failed nests (in the brackets number of nests recognized as depredated by pine marten (¹) and great spotted woodpecker (²)) of great tits in the study period 2002–2015.

		2002	2003	2004	2005	2006	2007	2008	2009	2010	2011	2012	2013	2014	2015	Total
Parkland	all nests	45	52	52	35	39	53	76	46*	34*	29*	43*	65	77	78	724
	failed nests	3	2	11	8	2	5	9	6	10	7	4	9	8	12	96
Forest	all nests	17	47	42	28	26	44	54	38	14*	31	55	39	58	58	551
	failed nests	0	2	17 (12)^1	2 (1)^2	8 (1)^2	15 (1)^2	16 (3)^1 (1)^2	6	6	5 (1)^2	8 (1)^2	6 (1)^2	6	4 (2)^2	101

*only clutches which were not subjected to the experiments (control group).

Data analyses

We used general linear models to compare the mean number of hatchlings and the mean number of fledglings between study areas and years. We applied a factorial design with the number of hatchlings and the number of fledglings as dependent variables in two separate models, where study area and year were factors, with their interaction being also included.

Hatching success, i.e. the number of hatchlings in relation to clutch size, and fledging success, i.e. the number of fledglings in relation to the number of hatchlings, were considered to represent binomial distribution. Therefore, we treated them as dependent variables in two corresponding generalized linear models, where study site and year were factors whose interactions were also included in the models. These generalized linear models with binomial error distribution, logit link function and Wald Chi-squared test statistics were used to examine differences in hatching success and in fledging success between two study areas (Crawley 2002). Linear correlations were calculated to analyze relationships between the number of fledglings, the number of hatchlings and clutch sizes. We also tested if there were associations of the breeding performance and weather variables, the richness of the food base for chicks or population density. This was done using linear regressions. Especially, we analyzed relationships between mean fledgling numbers per nest in a given year and mean temperatures of May, total rainfall in May, peak caterpillar abundance and density of breeding pairs. Modeling was conducted using IBM SPSS Statistics 22, while linear regression analyses were done applying Statistica 12 (StatSoft Inc. 1984–2014).

Results

Breeding characteristics

Over all years of the study, 13.3% of all initiated clutches failed in the urban park site, by comparison with 18.3% in the forest site. We did not record any depredated nests in the park site, whereas in the forest, almost 14,9% of the losses were caused by the pine marten (Martes martes) predation (2,7% of all nests), and 8,9% by great spotted woodpecker (Dendrocopos major) predation (1,6% of all nests). In the urban park site, the smallest percentage of failed nests was found in 2003 (3,8%) and the largest percentage in 2010 (29.4%). During the first study year in the forest site, 2002, no failed nest was recorded, but in 2003, 4.3% nets failed. The largest percentage of losses in the forest site occurred in 2010 (42.9%) and in 2004 (40.5%). Despite these extreme records, over all study years, percentages of totally failed nests were not correlated between study sites (r = 0.31; N = 14; p = 0.27).

In total, considering clutches that gave at least one hatchling, 90.5% eggs in the urban park and 92.3% eggs in the forest hatched. Analogously, 87.7% hatchlings in the urban park and 93.7% hatchlings in the forest fledged from broods that gave at least one fledgling.

The annual mean number of hatchlings per nest during the study period differed between the study areas and was higher in the forest site. The overall mean number of hatchlings was 8.29 ± 1.72 (SD) in the park site (the lowest mean 7.59 ± 1.65 in 2013 and the highest mean 8.77 ± 1.55 in 2008) and 9.51 ± 1.93 in the forest site (the lowest mean 8.00 ± 3.56 in 2005 and the highest mean 10.86 ± 1.55 in 2003), with a significant interaction between year and study area (Figure 2, Table II). In the forest area, year-to-year changes in the number of hatchlings were more substantial than in the parkland area. The mean number of fledglings also differed between the parkland and the forest study areas, with higher values occurring in the forest area. The overall mean number of fledglings was 7.12 ± 2.12 (the lowest mean 6.25 ± 1.85 in 2010 and the highest mean 8.31 ± 2.29 in 2002) in the parkland and 8.87 ± 2.21 (the lowest mean 7.31 ± 1.87 in 2005 and the highest mean 10.47 ± 1.84 in 2002) in the forest, with a significant interaction between year and study area (Figure 2, Table II), resulting from year-to-year changes being greater in the forest than the park site.

Table II. Summary of two general linear models testing for the effects of year and study area on, respectively, the number of hatchlings and the number of fledglings of great tits breeding in the forest and in the urban parkland study sites.

Y-variable and effects	df	F	p
The number of hatchlings
Intercept	1	225188	<0,0001
Year	13	6,3	<0,0001
Study area	1	89,0	<0,0001
Year x Study area	13	2,4	0,004
The number of fledglings
Intercept	1	127821	<0,0001
Year	13	7,9	<0,0001
Study area	1	131,6	<0,0001
Year x Study area	13	2,6	0,002

Figure 2. Annual variation of the mean number of great tit hatchlings (upper chart) and fledglings (bottom chart) in two study areas, a parkland and a forest (breeding seasons 2002–2015). Data are presented as means ± SE.

There was a positive relationship between the number of hatchlings and clutch size in both study sites: parkland (r = 0.76; n = 616; p < 0.001) and forest (r = 0.84; n = 463; p < 0.001). There was also a similar positive relationship between the number of fledglings and the number of hatchlings (parkland: r = 0.64; n = 569; p < 0.001; forest: r = 0.77; n = 407; p < 0.001).

The hatchability of eggs was affected by a significant interaction between study area and year (Table III, Figure 3), as only in some years hatching success was significantly different between the study sites and it was always higher in the forest (except 2013 year when was opposite). The same interaction had an impact on the fledging success (Table III, Figure 3) but in this case, differences in fledging success occurred often and almost always fledging success was higher in the forest.

Table III. Results of two generalized linear binominal models testing for the effects of year and study area on, respectively, hatching success and fledging success of great tits in the forest and the urban parkland study sites.

Y-variable and effects	df	Wald χ^2	p
Hatching success (N = 1079)
Intercept	1	3716,253	<0,0001
Year	13	23,480	0,04
Study area	1	6,457	0,01
Year x Study area	13	25,492	0,02
Fledging success (N = 976)
Intercept	1	2346,120	<0,0001
Year	13	107,852	<0,0001
Study area	1	62,053	<0,0001
Year x Study area	13	66,978	<0,0001

Figure 3. Mean hatching success (upper chart), fledging success (middle chart), and breeding success (bottom chart) of great tits in two study areas, a parkland and a forest (breeding seasons 2002–2015). Data are presented as means ± SE.

Breeding success

The annual mean number of fledglings per nest did not correlate with the annual peak caterpillar frass fall in the urban parkland, but there was a significant correlation in the forest (Table IV). The mean number of fledglings was not linked with the breeding pair densities (pairs/10 ha) in a given season in either study site. The mean number of fledglings was not linked with total rainfall in any study site either, but in the urban parkland, there was a non-significant negative tendency (Table IV). On the other hand, in both study areas, we found a significant positive relationship between the mean number of fledglings and mean May temperatures and, moreover, in the parkland, this correlation was high (Table IV, Figure 4).

Table IV. Correlations between mean fledgling numbers, mean fledging success, mean breeding success and four explanatory variables: maximum frass fall peak size, breeding densities, mean May temperature, May rainfall sum. Sample size for frass fall peak size N = 13; for the other variables N = 14.

		Frass fall peak size	Breeding densities	Mean May temperature	May rainfall sum
parkland	Fledgling numbers	r = 0.21; p = 0.49	r = −0.26; p = 0.37	r = 0.76; p = 0.002	r = −0.48; p = 0.08
	Fledging success	r = 0.16; p = 0.59	r = −0.34; p = 0.24	r = 0.69; p = 0.006	r = −0.29; p = 0.31
	Breeding success	r = 0.40; p = 0.18	r = 0.22; p = 0.45	r = 0.58; p = 0.03	r = −0.24; p = 0.42
forest	Fledgling numbers	r = 0.63; p = 0.02	r = 0.35; p = 0.21	r = 0.54; p = 0.046	r = −0,21; p = 0.46
	Fledging success	r = 0.43; p = 0.14	r = 0.11; p = 0.71	r = 0.29; p = 0.31	r = −0.04; p = 0.90
	Breeding success	r = 0.39; p = 0.19	r = 0.34; p = 0.23	r = 0.45; p = 0.1	r = −0.30; p = 0.30

Figure 4. Relationship between the mean number of great tit fledglings and mean May temperatures in the parkland and the forest (breeding seasons 2002–2015).

The mean fledging success and mean breeding success in the forest were not linked to any of the analysed variables, while in the case of the urban park site, fledging success and breeding success were consistently positively correlated with mean May temperatures (Table IV).

Discussion

In this study conducted in central Poland, we found that a proportion of clutches that totally failed (nests that ended at incubation stage or nests where all chicks died) was slightly lower in the urban park habitat than in the forest habitat. Symptomatically, the rate of failure changed among years independently in either study site. This suggests the impact of various and site-specific factors. Those losses had different reasons (e.g. starvation, soaking, predation), sometimes difficult to determine. One of the causes that could be relatively easily and correctly identified in the field was predation by the pine marten and great spotted woodpecker, which took place only in the forest site. The pressure exerted by these two predators clearly distinguished our two study areas, but the possibility of nest robbery by the predators was also strongly associated with the nest-box design (Skwarska et al. 2009; Kaliński et al. 2014). Similarly, nest predation by the weasel (Mustela nivalis) dependent on nest-box construction was observed in Wytham Wood, Oxfordshire, UK. In that case, the wooden nest-boxes had to be replaced with the concrete ones to avoid predation (Julliard et al. 1997). The literature on the pressure of predation in the context of the contrast between urban and non-urban environments is somewhat contradictory (Chamberlain et al. 2009; Vincze et al. 2017). Nonetheless, Vincze et al. (2017) have concluded that cavity nests are depredated at a significantly lower rate in urban than in rural habitats and it is in line with the situation observed in our urban-non-urban habitat system.

The number of hatchlings and hatching success are important characteristics of reproductive performance in birds and it is known that the number of hatchlings is usually directly related to the number of eggs in the clutch (Koenig 1982). Accordingly, we found high correlations between these two variables in both study sites. Temporal and spatial patterns of variation in the mean number of hatchlings we found were very similar to variation in mean clutch size that we had previously shown (Wawrzyniak et al. 2015), where clutch sizes of great tits were lower in the urban park than in the forest, mostly due to differences in the site-specific food abundance and patchy environment in the parkland. Our results on hatching success are congruent with the average hatching success across passerine birds, ca. 91% shown by Koenig (1982). This result is also similar to findings on other great tit populations studied in Europe, for example, 86,1–93,6% (Britt & Deeming 2011), 93% (Eeva & Lekihoinen 1995), but tends to be higher than in Frankfurt birds, 72–86% (Berresem et al. 1983), and Göteborg urban and rural populations, 79–80% (Isaksson et al. 2008).

In general, the hatchability of eggs was slightly higher in the forest than in the urban park site. Hatching success was relatively high and stable during the study period in both areas, with an exception occurring in 2010 in both places and 2006 at the park site. In the spring 2010, there was an unusually rainy period with very low temperatures (especially in May there were 24 rainy days and very high sum of rainfall, but also April was cold), which probably caused a large decrease in hatching success. In that breeding season, there was also the highest proportion of nests that completely failed in both study sites and the lowest fledging success in the urban parkland, but not in the forest where, however, only slightly more than half of the broods were successful. In general, hatching failure results from three major causes: female gametes fail to be fertilized, fertilized eggs fail to hatch, or calcium deficiency in the environment, that may cause eggshells to be thinner and prone to damage (Birkhead et al. 2008; Bańbura et al. 2010; Garcia-Navas et al. 2011). Embryo mortality may be caused by abiotic factors (variable temperature, humidity), female infectious disease, female condition or inbreeding (Kempenaers et al. 1996; Birkhead et al. 2008; Szulkin et al. 2012). Embryonic mortality can occur at any stage of development and for a variety of reasons, but generally may occur very early before egg-laying or late in the incubation period (Birkhead et al. 2008). Environmental factors, especially those associated with changes in temperature and humidity may impose embryo mortality in the period between egg-laying and hatching, and therefore, it seems that the abiotic factors could have a crucial role in the case of distinctly reduced hatching success like that in the 2010 year in our study.

Recent reviews of avian productivity and avian life-history evolution in the urban landscape context show equivocal findings (Chamberlain et al. 2009; Sepp et al. 2018). On the one hand, considering productivity (the number of fledglings) per successful nesting attempt Chamberlain et al. (2009) found a quite clear pattern of lower productivity in urban habitats in comparison to rural ones for majority of studied species, but this general rule was less apparent when they took in to account the number of fledglings from all attempts (also failed nests). Most European studies on great tits and blue tits have shown that forest populations produce more fledglings than urban populations (Berresem et al. 1983; Cowie & Hinsley 1987; Hőrak 1993; Riddington & Gosler 1995; Solonen 2001; Hinsley et al. 2008; Bailly et al. 2016; Glądalski et al. 2017; Pollock et al. 2017; de Satge et al. 2019). Charmantier et al. (2017) have not found any difference between tit populations nesting in the city of Montpellier (France) and in a nearby rural oak forest (but does not specify if all nests were included or only successful nests). Isaksson and Andersson (2007) found an opposite pattern around Göteborg, with urban tit populations being more productive than nearby forest ones.

This study shows a sustained pattern where the forest population of great tits produced more fledglings per successful nests and demonstrated higher breeding success over many breeding seasons. In our study system, breeding success was higher in the forest site in 13 out of 14 years. Fledging success also demonstrates a similar but slightly less obvious pattern, with higher values for forest than parkland area. The main reason for this interhabitat difference is probably a contrast in food availability and quality between the study habitats. Firstly, we have previously shown that mean clutch size was consistently lower in the parkland than in the forest great tit population, at least partly in response to the greater abundance of caterpillars in the forest (Wawrzyniak et al. 2015). Rodriguez et al. (2016) in a study of a Mediterranean great tit population breeding in an orange plantation concluded that the number of hatchlings per nest was the most important predictor of fledgling production.

Our study areas significantly differed in their insect productivity, including caterpillar productivity, with caterpillars being several times more abundant at the forest site than in the parkland site (Marciniak et al. 2007; Glądalski et al. 2015). In the forest site, the mean number of fledglings was related to the amount of frass fall but fledging success was not. It seems that the caterpillar numbers in the forest influenced fledgling numbers to a greater extent via clutch sizes than by lower chick mortality. In the caterpillar-poorer urban park habitat, neither fledgling numbers nor fledging success was correlated with the peak mass of frass fall Many studies on tits indicate a relationship between the number of fledglings or fledgling/breeding success and a lower quantity and/or quality of food provided to the offspring in urban habitats in comparison with rural habitats. Poorer food supplied to nestlings in urban habitats leads to a lower offspring number or breeding/fledging success (Cowie & Hinsley 1987; Hőrak 1993; Solonen 2001; Bailly et al. 2016; Pollock et al. 2017). In some cases, the opposite effects were found, where an urban habitat was richer and, as a consequence, tit breeding performance was better there (Isaksson & Andersson 2007). Generally, it has been shown that great tits can cope with it by adjusting parental effort; however, it is hard to clearly define the mechanisms which are responsible for that. Because on the one hand it is possible that suboptimal habitat attracts poorly performing individuals and that there may be a genetic determinant beyond habitat selection and exploration abilities (for example Dingemanse et al. 2002; Carere et al. 2005). On the other hand, it is also possible that parents are able to adjust their breeding strategies to different habitat conditions (for example, Caprio & Rolando 2017) and it is very likely that both mechanisms matter. Connections between habitat, food richness and breeding performance in of tits seem to form a more universal phenomenon, not limited to just urban-rural gradient, but also to other food-contrasted habitat types (Blondel et al. 1987; Lambrechts et al. 1997; Massa et al. 2011). In caterpillar-poor habitats like coniferous forests, sclerophyllous forests, reforestations, orange plantations or, finally, urban habitats, great and blue tits not only lay fewer eggs but also are forced to use alternative prey taxa of invertebrates instead of caterpillars to feed the chicks (Blondel et al. 1991; Bańbura et al. 1994; Naef-Daenzer et al. 2000; Solonen 2001; Tremblay et al. 2003; Massa et al. 2004, 2011). From our previous study and from a study in progress we know that in the urban park site great tits used alternative insect prey as nestling food to a greater extent, although caterpillars were still the dominant prey (Michalski et al. 2011). These observations suggest that caterpillar abundance may not be as important to great tit breeding success at the park site. Because of nutrient deficiencies, switching to alternative prey may negatively affect either the survival of the chicks or their condition or both, especially when other important factors are also unfavorable (van Balen 1973; Naef-Daenzer & Keller 1999; Barba et al. 2004; Mackenzie et al. 2014; Kaliński et al. 2015b).

In complex ecological systems, it is unlikely that one factor, even so important for tits as the abundance of caterpillars could determine the breeding performance of birds and most probably other factors like habitat structure, weather conditions, human-induced effects or breeding densities must also directly or indirectly influence breeding results (Bańbura et al. 1994; Zając 1995; Hinsley et al. 2008). Bueno-Enciso et al. (2016) showed that the micro-habitat surrounding nest sites and the size of the forest patch in a patchy forest area are important components of habitat quality for breeding tits, with habitat quality being a reliable index of prey availability for insectivorous birds. Mackenzie et al. (2014) found a positive relationship between the number of oak trees near the nest and the fledgling weights in great tits and pointed out the importance of native vegetation for the foraging style. Hinsley et al. (2008) showed that tits in a patchy environment in territories with a lower number of oaks and more gaps in canopy worked harder to raise their nestlings that finally were lighter anyway. de Satge et al. (2019) found that a proportion of eggs that gave fledglings was negatively influenced by local-scale urbanisation, quantified by percentage of built up area. The vegetation in our urban parkland is heavily fragmented by lawns, paths and buildings, and it was mainly formed artificially (Marciniak et al. 2007). The density of trees (especially oaks) in the urban park area is much lower than in the forest (and the trees are not as mature as trees in the forest area), and, moreover, there are many non-native deciduous and coniferous trees (Glądalski et al. 2017). It is likely that all those factors synergistically impose worse breeding performance of the great tits in the urban park site.

It can be assumed that a high density of breeding pairs may lead to a decrease in breeding success. This may be due to, e.g. reducing the size of territories, more frequent aggressive interactions between individuals or easier transfer of parasites and pathogens. Some studies of European nest-box tit populations, where the density of breeding pairs was high, reported negative impact of densities on clutch size or other breeding indicators (Kluijver 1951; Perrins 1965; van Balen 1973; Dhondt 2010). Also, some experimental studies showed such a negative impact (Dhondt et al. 1992; Both 1998). Densities of great tits in our parkland and forest areas were rather low or medium and much lower than reported for most west-European nest-box populations of this species (Perrins 1965; van Balen 1973; Dhondt 2010). Dhondt (2010) analyzed several Belgian tit populations for many years and concluded that density-dependent factors that affected tit reproduction are more likely to be detected in low quality sites than in high quality ones. Therefore, we expected that density-dependent effects influencing the breeding performance in our study should be small, negligible or limited rather to the urban park site. Indeed, we found no significant correlations between the breeding densities and mean numbers of fledglings or fledging success in our study sites. Despite this, it needs to be highlighted that the nest-box breeding density of great tits differed between the two study sites and was distinctly higher in the urban park every year, being nearly twice as high as in the forest area (Glądalski et al. 2016c).

Weather conditions during incubation and, especially, during the nestling stage may strongly affect breeding performance directly or indirectly (van Balen 1973; Martin 1987). On the one hand, low temperatures increase nestling energy demands, especially when air humidity is high. Additionally, intensive rainfall, which can lead to getting the nest material wet enhances this effect. Furthermore, temperature and heavy rainfall can influence prey abundance and availability for both adult and nestling tits (Southwood et al. 2004). In the present study, in the urban park site, annual mean fledgling numbers, fledging success, and breeding success were significantly positively correlated with mean daily temperatures in May. Fledgling numbers tended to be negatively correlated with rainfall sum in May. In the forest site, there was no such strong effect, and the fledgling number was significantly positively related only with mean May temperatures. Similarly, breeding success tended to be related to temperature, but fledging success did not. It is possible that in the low-quality parkland area unfavorable weather conditions may exert stronger pressures on adult birds and their nestlings. Thus, a different response of fledging success to roughly the same weather conditions at two study sites may be an indirect consequence of the difference between these habitats in their trophic richness. However, also microclimatic conditions might be slightly different, as a result of site-specific habitat features. For example, it seems that patchy structure of the habitat caused more frequent nest wetting in the urban park site in periods of heavy and prolonged rainfalls (own observations). A similar but not exactly the same pattern with a strong positive correlation between the nestling hemoglobin concentration and mean minimum daily temperatures during the nestling period within the park site, but with no relationship in the forest site, was previously shown in our study system (Kaliński et al. 2015b). It is in line with the results presented in this study, regarding the fledging successes. We did not find such differences in the case of fledgling numbers, perhaps because the numbers of fledglings were strongly connected with clutch sizes and hatchling numbers. Radford et al. (2001) showed that female great tits significantly reduced their feeding visit rate to the nest during intensive rainfall. Lower breeding performance connected with unfavorable weather conditions that increased mortality of young great tits has been presented previously (Zając 1995).

Conclusions

We found a clear, consistent, long-term spatial pattern where a forest population of great tits produced more hatchlings and fledglings per successful nest and was characterized by higher breeding success than an urban park population. It may result from such habitat differences as tree species composition and spatial structure, and corresponding caterpillar abundance. Other factors may also be relevant, e.g. human disturbance indicated by the density of pathways. Annual mean number of fledglings per a successful nest was positively linked to caterpillar richness only in the forest site. On the other hand, higher temperatures during chick rearing in May were associated with a greater number of fledglings and fledging success in the parkland site, but only with a greater number of fledglings in the forest. The between-population variation we found probably reflects a more general difference between urban and forest populations of tits.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures using animals were authorized under permits from the University of Łódź, Local ethical Committe and the State Office for Environmental Protection.

Acknowledgements

We thank E. Wróblewska, A. Jaksa, D. Mańkowska, M. Janiszewska and J. Białek for collaboration and consents.

Disclosure statement

The authors declare that they have no conflict of interest.

Additional information

Funding

The study was funded by a grant from the National Science Centre Poland No. N N304 045136, University of Łódź (B161100000006101).