| | Received: 18 March 2019    Revised: 17 January 2020    Accepted: 31 January 2020 DOI: 10.1111/jbi.13830 RE SE ARCH PAPER The roles of temperature, nest predators and information parasites for geographical variation in egg covering behaviour of tits (Paridae) Olli J. Loukola1,2  | Peter Adamik3  | Frank Adriaensen4 | Emilio Barba5  | Blandine Doligez6  | Einar Flensted-Jensen7 | Tapio Eeva8  | Sami M. Kivelä1  | Toni Laaksonen8  | Chiara Morosinotto9  | Raivo Mänd10  | Petri T. Niemelä11  | Vladimir Remeš3,12  | Jelmer M. Samplonius13,14  | Manrico Sebastiano15,16  | Juan Carlos Senar17  | Tore Slagsvold18  | Alberto Sorace19 | Barbara Tschirren20  | János Török21  | Jukka T. Forsman1,22 1 Department of Ecology and Genetics, University of Oulu, Oulu, Finland 2 Botanical Museum, Biodiversity Unit, University of Oulu, Oulu, Finland 3 Laboratory of Ornithology, Department of Zoology, Palacky University, Olomouc, Czech Republic 4 Department of Biology, Evolutionary Ecology Group, University of Antwerp, Antwerp, Belgium 5 Terrestrial Vertebrates Research Unit “Cavanilles”, Institute of Biodiversity and Evolutionary Biology, University of Valencia, Paterna, Spain 6 CNRS, Department of Biometry & Evolutionary Biology, UMR 5558, University of Lyon 1, University of Lyon, Villeurbanne, France 7 Cypresvej 1, Brønderslev, Denmark 8 Department of Biology, University of Turku, Turku, Finland 9 Bioeconomy Research Team, Novia University of Applied Sciences, Ekenäs, Finland 10 Institute of Ecology & Earth Sciences, University of Tartu, Tartu, Estonia 11 Department Biologie II, LMU-München, Munich, Germany 12 Department of Ecology, Charles University, Praha, Czech Republic 13 Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands 14 Institute of Evolutionary Biology, The University of Edinburgh, The King’s Buildings, Edinburgh, UK 15 Behavioural Ecology and Ecophysiology Group, Department of Biology, University of Antwerp, Wilrijk, Belgium 16 Centre d’Études Biologiques de Chizé (CEBC), UMR 7372 CNRS-Université de La Rochelle, Villiers-en-Bois, France 17 Evolutionary and Behavioural Ecology Unit, Museu de Ciències Naturals de Barcelona, Barcelona, Spain 18 19 Department of Biosciences, University of Oslo, Oslo, Norway ISPRA, Rome, Italy 20 Centre for Ecology and Conservation, University of Exeter, Penryn, UK 21 Department of Systematic Zoology and Ecology, Behavioural Ecology Group, Eötvös Loránd University, Budapest, Hungary 22 Natural Resources Institute Finland (Luke, Oulu), University of Oulu, Oulu, Finland Correspondence Olli J. Loukola, Department of Ecology and Genetics, University of Oulu, Oulu, Finland. Email: olli.loukola@oulu.fi Abstract Aim: Nest building is widespread among animals. Nests may provide receptacles for eggs, developing offspring and the parents, and protect them from adverse environmental conditions. Nests may also indicate the quality of the territory and its owner This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Journal of Biogeography published by John Wiley & Sons Ltd. Journal of Biogeography. 2020;00:1–12.  | wileyonlinelibrary.com/journal/jbi     1 | 2       Funding information Biotieteiden ja Ympäristön Tutkimuksen Toimikunta, Grant/Award Number: 122665, 125720, 24302601, 314833 and 319898; Agencia Estatal de Investigación, Ministry of Economy, Industry and Competitiveness, Spanish Research Council, Grant/Award Number: CGL-2016-79568-C3-3-P; Koneen Säätiö; Biological Interactions Doctoral Programme; Jenny ja Antti Wihurin Rahasto Handling Editor: Lisa Manne LOUKOLA et al. and can be considered as an extended phenotype of its builder(s). Nests may, thus, function as a sexual and social signal. Here, we examined ecological and abiotic factors—temperature, nest predation and interspecific information utilization—shaping geographical variation in a specific nest structure—hair and feather cover of eggs— and its function as an extended phenotype before incubation in great (Parus major) and blue tits (Cyanistes caeruleus) across Europe. We also tested whether egg covering is associated with reproductive success of great tits. Location: Fourteen different study sites and 28 populations across Europe. Taxon: Parus major, Cyanistes caeruleus. Methods: We recorded clutch coverage estimates and collected egg covering nest material from the tit nests. We also measured nest specific breeding parameters and phenotypic measurements on adults. We tested whether mean spring temperatures, nest predation rates and flycatcher (Ficedula spp) densities in the study areas explain the large-scale geographical variation of clutch coverage and reproductive success of tits. Results: The degree of egg coverage of great tits increased with lower mean spring temperature, higher nest predation rate and higher flycatcher density. We did not find egg covering of blue tits to be associated with any of the ecological or abiotic factors. Moreover, egg covering of great tits was not associated with reproductive success in our cross-sectional data, yet a rigorous assessment of fitness effects would require long-term data. Main conclusions: Our findings suggest that, in great tits, egg covering may simultaneously provide thermal insulation against cold temperatures during egg-laying in spring and also represent a counter-adaptation to reduce information parasitism by flycatchers and nest predation. Hence, geographical variation in interspecific interactions, and consequently in co-evolutionary processes, may affect the evolution of nest characteristics besides environmental conditions. KEYWORDS bird nest, breeding success, Cyanistes caeruleus, extended phenotype, nest structure, Parus major 1 |  I NTRO D U C TI O N (Grubbauer & Hoi, 1996; Hoi, Schleicher, & Valera, 1994; Jelínek, In the animal kingdom, nest building is a common behaviour. The nal in mate attraction and selection (Schaedelin & Taborsky, 2009). basic functions of nest building are thought to be protection against In black kites (Milvus migrans), the decoration of nests with pieces elements of abiotic (e.g. low temperatures, humidity) and biotic of white plastic is a reliable signal in dominance hierarchy among (e.g. nest predators, parasites) risks for offspring until they hatch conspecifics (Sergio et al., 2011). Thus, a perceptible nest can be or become independent from parental care (Hansell, 2007). Nest considered an extended phenotype of its builder(s) (Dawkins, 2016), structure shows large variation across species. Some species invest because the placement, structure, materials and size of the nest af- a considerable amount of time and resources in building complex fects the probability that the genes of the builder(s) are transmitted and decorated nest structures while, in others, just a few pieces to the next generation by affecting mate selection and offspring of rock or plant material are enough (Hansell, 2007). This implies survival probability. Požgayová, Honza, & Procházka, 2016), the nest has become a sig- that nests may also have functions other than offering security to Extended phenotypes, such as odour, chemical marks, nests offspring during development. In some species, such as the stickle- and other constructions (webs, excavations, burrows, bowers, back (Gasterosteus aculeatus) (Barber, Nairn, & Huntingford, 2001; piles or pieces of various materials), are often important signals in Östlund-Nilsson & Holmlund, 2003), cichlid fishes (McKaye, Louda, intentional communication among conspecifics related to mate at- & Stauffer, 1990; Schaedelin & Taborsky, 2006) and passerines traction and selection, dominance hierarchy, territory defence and |       3 LOUKOLA et al. species recognition (Schaedelin & Taborsky, 2009). These signals Second, the nest predation hypothesis postulates that egg cov- may also be long-lasting and readily available to heterospecifics, ac- ering is a protection against nest predators (Haftorn & Slagsvold, tually providing a source of inadvertent information about the loca- 1995; Saavedra & Amo, 2019) or interspecific competitors that tion, decisions, social structure and dominance, body condition, and may damage the nest. For example, recent experiment by Saavedra cognitive capabilities of signal producers to those who can interpret and Amo (2019) showed that blue tits covered their eggs more fre- the signals. For example, in bowerbirds (family Ptilonorhynchidae), quently when they detected an increase in the perceived risk of the elaborateness of the display structure, the bower, reflects the predation. Kreisinger and Albrecht (2008) showed experimentally species identity and also the age and experience of the focal male that mallard (Anas platyrhynchos) nests that were covered with nest (Vellenga, 2016). Both con- and heterospecifics may thus use it to material, suffered significantly lower rates of nest predation than make inferences about the quality of the territory and its owner. nests which were left uncovered. An example of the interspecific The use of inadvertent information is common among conspecif- competition is found in house wrens (Troglodytes aedon) in North ics (Danchin, Giraldeau, Valone, & Wagner, 2004) but also among het- America that may destroy the nests of black-capped chickadees erospecifics (Seppänen, Forsman, Mönkkönen, & Thomson, 2007). (Poecile atricapillus) and tufted titmice (Baeolophus bicolor; White & Most valuable interspecific information is predicted to be provided Kennedy, 1997). In general, nest predation is a major factor affect- by species with overlapping resource needs (Seppänen et al., 2007). ing the behaviour and life history traits in birds (Martin & Briskie, Many traits defining extended phenotypes have been shown or sug- 2009). gested to be used by heterospecifics as sources of information: tit Finally, the most recent hypothesis, the information parasitism (Paridae) clutch size by flycatchers (Ficedula spp) for breeding habitat hypothesis, suggests that great tits cover eggs to protect against selection (Forsman & Seppänen, 2011; Loukola, Seppänen, Krams, information acquisition by flycatchers (Loukola et al., 2014). Upon Torvinen, & Forsman, 2013; Samplonius, Kappers, Brands, & Both, arrival, migratory flycatchers are attracted to the proximity of 2016; Seppänen & Forsman, 2007; Seppänen, Forsman, Mönkkönen, resident tits during their nest-site selection that results in fitness Krams, & Salmi, 2011), sibling vole's (Microtus levis) odour and chem- benefits (Forsman, Seppänen, & Mönkkönen, 2002) and the visi- ical signals by field voles (Microtus agrestis) for predator avoidance ble clutch size of tits seems to be an important source of informa- (Hughes, Korpimäki, & Banks, 2010) and stingless bee's (Melipona ru- tion for flycatchers. In general, the tits are still in egg-laying stage fiventris) odour and chemical signals by another stingless bee species when the Flycatchers prospect tits’ nests in spring (Forsman et al., (Trigona spinipes) for space use and foraging decisions (Nieh et al., 2018; Forsman & Thomson, 2008; Samplonius & Both, 2019) and 2004). However, in contrast to bodily phenotypes, we know very may use tit clutch size to adjust their own investment in the off- little about geographical variation of extended phenotypes (but see spring (clutch size and egg mass) (Forsman, Seppänen, & Nykänen, Deeming & Mainwaring, 2015; Hansell, 2000) and the potential pro- 2011), and in deciding whether they would copy or reject nest-site cesses behind the patterns. preferences of the focal tits (Forsman & Seppänen, 2011; Loukola Tits’ distribution ranges are large, and thus, their nesting be- et al., 2013; Seppänen et al., 2011). Flycatchers’ interest in the haviours provide a good model system to examine large-scale geo- clutch size of tits makes sense as environmental variation explains graphical patterns of extended phenotypes. All tit species are cavity a large amount of variance in clutch size in blue tits (e.g. Tremblay, nesting, and the basic structure of the nest consists of moss and a Thomas, Lambrechts, Blondel, & Perret, 2003) and great tits (e.g. layer of animal hair or feathers on top, on which eggs are laid. During Beldal et al., 1998), implying that tit clutch size reliably reflects the egg-laying, eggs are usually covered with a loose tuft of hair, feath- quality of the environment and/or parents and can readily be used ers, moss, hay or other light material. This characteristic, the cover- as a cue on territory quality. Thus, tit nests can be considered to ing of eggs, is our trait of interest because it occurs widely in genus include two components of an extended phenotype that are used Parus and Cyanistes (Haftorn & Slagsvold, 1995), yet the propensity by information parasites: clutch size (reflecting parental/territorial to cover the eggs varies both among individuals within populations quality) and nest structure that covers the clutch totally, partially and among geographically distinct populations (Loukola, Laaksonen, or not at all. Seppänen, & Forsman, 2014). In great tits, usually all eggs are totally The information utilization by flycatchers is not neutral to tits. covered with hair, but sometimes the cover is partial or does not The selective copying of nest-site characteristics by flycatchers exist at all (Loukola et al., 2013). may lead to niche convergence (Loukola et al., 2013) and results Three mutually non-exclusive hypotheses have been put for- in fitness losses in great tits in terms of the number and condition ward to explain great and blue tit nest structure and egg covering of fledglings (Forsman, Thomson, & Seppänen, 2007). Once fly- behaviour (Haftorn & Slagsvold, 1995). First, the insulation hypothesis catchers (i.e. the information parasite) have evolved a strategy for predicts that the cover provides thermal insulation against cold tem- taking advantage of a tit (i.e. the host), tits are expected to evolve peratures during egg-laying in spring. Indeed, recent studies show counter-adaptations, which may lead to an evolutionary arms race that the mass and insulation capacity of great and blue tit nests are (Dawkins & Krebs, 1979) between the tits and the flycatchers on lower at high ambient temperature (Deeming, Mainwaring, Hartley, acquiring and hiding information (Seppänen et al., 2007). Indeed, & Reynolds, 2012; Mainwaring, Hartley, Lambrechts, & Deeming, a recent study by Loukola et al. (2014) experimentally demon- 2014). strated that the simulated presence of pied flycatchers increased | 4       LOUKOLA et al. the amount of hair great tits brought on the eggs and covered them more carefully when exposed to flycatcher playback song compared to the control treatment with a playback song of a non-information-parasitic species. Thus, great tits’ nest structure and covering eggs with hair may also be a counter-adaptation to reduce information parasitism. Phenotypes (bodily and extended) often show geographical variation suggesting spatial variation in selection regimes (Mayr, 1956; Slatkin, 1973). The nests of birds make no exception (Deeming & Mainwaring, 2015; Hansell, 2000). Comparing egg covering behaviour of great and blue tits among different populations at a large geographical scale facilitates testing the insulation, nest predation and information parasitism hypotheses. This is because each of temperature during egg-laying period, the abundance of nest predators and potential information parasites (flycatchers) of tits vary geographically. As we do not know whether the hypothesized mechanisms have additive or interactive effects on egg covering behaviour, we test our hypotheses based on these perspectives; if the insulation, nest predation and information parasitism have additive effects on egg covering behaviour, the extent of egg covering should increase with lower mean spring temperature and higher nest predation rate. Based on results of Loukola et al. (2014), we also predict an increased extent of egg covering in the presence and density of potential information parasites. If there is an interactive component in how the hypothesized mechanisms affect egg covering behaviour, F I G U R E 1   A map of Europe showing the locations of the study areas. See Table S1 for more details concerning the study populations interactions among mean spring temperature, nest predation rate and density of information parasites should be found in statistical analysis. In addition to main hypotheses, other variables, such as nest floor area and habitat type, may affect tits egg covering behaviour. of the 28 populations. All study populations breed in nest boxes. Research was carried out in accordance with legislation of each country. Tits establish the fully lined nest cup only at the start of incubation (Deeming, Morton, & Laverack, 2019). If the eggs are spread out over a wider area in nest boxes with larger floor area, we ex- 2.2 | Field procedure pect that more material is needed to cover the eggs. If the density and the species composition of local bird and mammal communities, Nest building state and the beginning of the egg-laying (laydate) which are linked to various characteristics of the habitat, including were checked during regular field observations. Use of egg cover tree species, affect the availability of feathers and hairs (egg cover- tends to increase during the first day of the laying stage (Haftorn ing material), we expect to find differences in the extent of egg cov- & Slagsvold, 1995). During the egg-laying stage, when tits had laid ering in study sites with different habitat types. Finally, we explore their fourth to eighth egg, (a) the nest was photographed to get whether reproductive success of the tits (number of hatched eggs a measurement of the extent of the clutch coverage, that is, the and fledglings) is positively associated with extent of egg covering, proportion of the visible clutch surface (%) and (b) all the hair and as would be expected if egg covering behaviour is under positive other material that covered tit eggs and nest cup was removed to natural selection. expose the eggs and placed in a zip lock bag for later measurement of hair mass and the nest was photographed again. After photo- 2 |  M ATE R I A L S A N D M E TH O DS 2.1 | Study areas graphing the nest, the removed material was replaced by same quantity of sheep hair. The onset of incubation was determined by observing the presence of female on the nest and touching eggs to determine whether the eggs were cold or warm. Nest specific breeding parameters (number of hatched eggs and fledglings) The great tit data for this study were collected in spring 2013 from and phenotypic measurements on adults (Table 1) were also col- 10 different countries, 14 study areas (Figure 1, Table S1) and 28 lected. We recorded clutch coverage estimates and mean spring populations in Europe. The blue tit data were collected in the same temperatures (from the nearest available meteorological stations year from 6 of the 10 countries, 8 of the 14 study areas and 22 to each of the study area) from 476 great tit nests and 123 blue |       5 LOUKOLA et al. TA B L E 1   List of variables. Model sets refer to the different sets of models that were used in assessing the study hypotheses (see Statistical methods section for details) Name of the variable Model set Type of the variable Definition of the variable Clutch coverage 1–5, 10, 6–9 Response explanatory First principal component of clutch covering rate and the mass of the covering material Number of hatched eggs 6, 7 Response   Number of fledglings 8, 9 Response   Dominant tree genus in the study area 1–5, 10 Explanatory Defines the habitat type. Affects egg covering material availability Age of the tit parent(s) 6–9 Explanatory Binary variable; 1-year-old or older Flycatcher density 1–9 Explanatory Proportion of nest boxes occupied by flycatchers in the study area. Standardized in model sets 6–9 Flycatcher presence 10 Explanatory Binary variable; flycatcher present or not Mean spring temperature 1–9, 10 Explanatory Mean daily temperatures (°C) between the beginning of the nest building and fledging, from the nearest available meteorological stations to each of the study area. Standardized in model sets 6–9 Clutch size 6–9 Explanatory Final number of eggs in the nest Nest predation rate 1–10 Explanatory The proportion of predated nests within a study site. Standardized in model sets 6–9. Nests where devices had been added to prevent nest predation (e.g. wire netting) were removed from the analysis Study population 1–5, 10 Random factor   Nest floor surface 1–5, 10 Explanatory Surface area of the nest box floor in cm2. Standardized in model sets 4 and 5 Geographical location 1–5, 10 Explanatory First principal component of altitude, latitude and longitude tit nests and nest predation rates from 345 great tit nests and 2.4 | Statistical methods 74 blue tit nests. Flycatcher (either Ficedula hypoleuca or Ficedula albicollis) density was measured in the end of breeding season as The distribution of clutch covering rate (proportion of covered eggs) the proportion of nest boxes occupied by flycatchers in the study was slightly U-shaped with a high peak at one (all eggs covered), population. which is problematic for analysis. Therefore, we measured clutch coverage by combining clutch covering rate and the mass of material 2.3 | Measurement of nest characteristics used to cover the eggs, because these variables together measure the investment of the tit parents in covering their clutch. For this purpose, we ran principal component analysis for the data on egg The clutch coverage rate was measured by comparing the propor- coverage and the mass of the covering material and used the first tions of the visible clutch surfaces from the digital photographs principal component (‘clutch coverage’ hereafter, explains 72.3% of taken from the nest before and after cover removals using Image J the variance, eigenvalue = 1.0) as a response variable when analysing software (US National Institutes of Health, http://imagej.nih.gov/ij). variation in clutch covering behaviour. Clutch coverage variable was The clutch surface was measured using freehand tracing and area symmetrically (approximately normally) distributed, and positively calculator tools. Clutch surfaces were measured twice from each correlated with both clutch covering rate and mass of the covering picture to minimize measurement error and average values were material, higher values, thus, indicating higher investment in clutch used in the analyses. Masses of the collected hair samples were covering (Figure S1). weighed to the nearest 0.0001 g by using an Ohaus AS120S analyti- All statistical analyses were conducted with R version 3.4.3 (R cal balance. Phenotypic measurements on adult tits were obtained Core Team, 2017). Linear mixed-effects models (LMMs; function when they were captured during food provisioning. Age was clas- lme in package ‘nlme’ (Pinheiro et al., 2017)) were used to analyse sified in the field as 1-year-old (second calendar year) or older (at variation in the clutch covering of great (Model sets 1–4) and blue least third calendar year) (Jenni & Winkler, 1994). Adult and young tits (Model set 5). Generalized linear mixed-effects models (func- birds were handled under the ringing licenses of the authors. Hence, tion glmer in package ‘lme4’; Bates, Mächler, Bolker, & Walker, 2014) our study complied with the national legislation of Belgium, Czech with Poisson distribution and a logarithmic link function were used Republic, Denmark, Estonia, Finland, Hungary, Italy, Spain, Sweden to analyse variation in the number of hatched eggs and fledglings of and Switzerland concerning handling wild animals. Variables used in the great tits (Model sets 6–9). In model sets 6–9, we standardized statistical analyses are listed in Table 1. all continuous explanatory variables of the model. Standardization | 6       LOUKOLA et al. makes the quantitative interpretation of model parameters less component of geographical variables (altitude, latitude and longi- intuitive, which is the reason why standardization was used only tude) and dominant tree genus in the study site were set as fixed when it was really needed for aiding/facilitating model conver- effects, and population as a random effect in the global model. Time gence. We used multi-model inference; effects of analysed vari- of the year (Laydate) was not included in the analysis because it is ables were summarized by model averaging (Burnham & Anderson, strongly negatively correlated with the first principal component 2002) (function model.avg in package ‘MuMIn’; Barton, 2009). of geographical variables (Pearson's correlation, r = −.61, t = −3.41, We derived 10 model sets. Model set 1 (Table 2a) tested if the df  =  343, p  <  .001) (see Laydate in Table S3). Nest predation rate alternative hypotheses (i.e. insulation, nest predation, information positively correlates with mean spring temperature (r = .67) but both parasitism), nest floor surface area or forest type (dominant tree of these variables were retained in all models because of their im- genus) in the study site explain variation in clutch coverage in great portance for assessing the study hypotheses. No interactions were tits. This model set was fitted to data (Nobservations = 341) including included in any model. The set of all meaningful models simpler than observations from all the study sites, also including sites where the the global model was derived with the function ‘dredge’ (package flycatcher density was zero. Mean spring temperature, nest preda- ‘MuMIn’; Bartón & Barton, 2017) for model averaging, the global tion rate, flycatcher density, nest floor surface area, first principal model being included in model averaging (see Table S2a for the set TA B L E 2   Model-averaged (full average) fixed effects in model sets 1 and 2 explaining clutch coverage in the great tit. Model set 1 is based on the assumption that temperature, nest predation and information parasitism act additively on clutch coverage, whereas interactive effects of these variables were assumed in model set 2 Model set Variables Estimate Adjusted SE z value (a) Model set 1 (Intercept) Pr(>|z|) 1.078 0.556 1.939 0.053 Nest floor surface 0.009 0.003 3.527 <0.001 Predation rate 0.045 0.015 3.075 0.002 Temperature −0.238 0.046 5.145 <0.001 DTG (Citrus) 1.750 0.608 2.876 0.004 DTG (Fagus) −0.754 0.679 1.110 0.267 DTG (Mixed) 0.037 0.541 0.069 0.945 DTG (Picea) −0.490 0.427 1.149 0.251 DTG (Pinus) 0.044 0.418 0.105 0.917 DTG (Quercus) 0.486 0.933 0.351 0.007 0.010 0.686 0.492 Geographical location (b) Model set 2 with interactions −0.453 Flycatcher density 0.093 0.184 0.505 0.614 (Intercept) 1.214 0.643 1.888 0.059 0.010 0.003 2.991 0.003 Predation rate −0.013 0.079 0.163 0.870 Temperature −0.276 0.085 3.246 0.001 DTG (Citrus) 1.988 0.709 2.805 0.005 DTG (Fagus) −0.767 0.666 1.151 0.250 DTG (Mixed) 0.094 0.568 0.166 0.868 Nest floor surface DTG (Picea) −0.482 0.427 1.129 0.259 DTG (Pinus) 0.091 0.427 0.213 0.831 −0.429 0.491 0.875 0.382 Flycatcher density DTG (Quercus) 0.010 0.026 0.406 0.685 Geographical location 0.074 0.172 0.429 0.668 Predation rate: Temperature 0.004 0.006 0.723 0.470 Flycatcher density: Temperature 0.000 0.002 0.138 0.890 Flycatcher density: Predation rate 0.000 0.001 0.101 0.920 Flycatcher density: Predation rate: Temperature 0.000 0.000 0.029 0.977 Note: Bold values indicates statistical significance. Geographical location = First principal component of altitude, latitude and longitude. Abbreviation: DTG, dominant tree genus. |       7 LOUKOLA et al. TA B L E 3   Model-averaged (full average) fixed effects of model sets 3 and 4 explaining clutch coverage in the great tit in study sites where the flycatchers were present. Model set 3 is based on the assumption that temperature, nest predation and information parasitism act additively on clutch coverage, whereas interactive effects of these variables were assumed in model set 4 Model set Variables Estimate Adjusted SE z value Pr(>|z|) (a) Model set 3 without interactions (Intercept) −1.241 1.182 1.050 0.294 Flycatcher density 0.036 0.014 2.591 0.010 Predation rate 0.022 0.014 1.547 0.122 Temperature −0.049 0.077 0.634 0.526 0.000 0.002 0.220 0.826 DTG (Picea) −0.001 0.217 0.003 0.997 DTG (Pinus) −0.026 0.181 0.142 0.887 DTG (Quercus) −0.003 0.279 0.010 0.992 0.009 0.111 0.085 0.932 −1.040 1.942 0.536 0.592 0.033 0.033 1.014 0.310 0.027 0.134 0.204 0.838 −0.065 0.172 0.378 0.706 Nest floor surface Geographical location (b) Model set 4 with interactions (Intercept) Flycatcher density Predation rate Temperature 0.001 0.003 0.257 0.798 DTG (Picea) Nest floor surface −0.004 0.219 0.016 0.987 DTG (Pinus) −0.032 0.306 0.103 0.918 DTG (Quercus) −0.006 0.351 0.018 0.985 Geographical location 0.010 0.131 0.074 0.941 Predation rate: Temperature 0.000 0.004 0.049 0.961 Flycatcher density: Predation rate 0.000 0.002 0.008 0.994 Flycatcher density: Temperature 0.000 0.003 0.030 0.976 Note: Bold values indicates statistical significance. Geographical location = First principal component of altitude, latitude and longitude. Abbreviation: DTG, dominant tree genus. of averaged models). Bivariate correlations between the study vari- tits (see Table S6 for the set of averaged models). Because of the ables are provided in Table S3. low number of blue tit observations, we did not conduct any further Model set 2 (Table 2b) was derived otherwise similarly to model analyses for this species. set 1, but all possible interactions among the nest predation rate, Model sets 6 and 7 tested whether the clutch coverage of great mean spring temperature and flycatcher density were included in tits or the ecological and abiotic environment explain the number of the global model (see Table S2b for the set of averaged models). hatched eggs of great tits by using all great tit data. Model set 3 (Table 3a) was derived otherwise similarly to In model set 6 (Table S7), number of hatched eggs was used as a model set 1, but these models were fitted to data including only dependent variable and clutch size was added as a covariate in the areas where the flycatchers were present (flycatcher density  >  0, global model in both model sets to take the effect of clutch size Nobservations = 169, see Table S4a for the set of averaged models). This variation into account. In addition to clutch size, fixed effects of was done to reliably estimate the effect of flycatcher density. In the the global models included also clutch coverage, mean spring tem- full data the high number of zeros (flycatchers not present) might perature, nest predation rate, flycatcher density, as well as female confound the estimation (underestimation) of flycatcher density ef- age and its interaction with clutch size, because female age affects fect on great tit egg covering behaviour. clutch size (Perrins & Mccleery, 1985). Population was set as a ran- Model set 4 (Table 3b) was derived otherwise similarly to model dom effect. Except clutch size (a non-negative integer), continuous set 3, but all two-way interactions among the nest predation rate, variables were standardized (by subtracting mean from each ob- mean spring temperature and flycatcher density were included in servation and dividing this difference by standard deviation, see the global model (the three-way interaction was ignored as the mod- Table S8 for the set of averaged models) to aid model convergence. el-fitting failed when it was included in the global model; see Table S4b for the set of averaged models). Model set 5 (Nobservations = 74; Table S5) was otherwise similar to model set 1, but it focused on variation in clutch coverage in blue Model set 7 (Table S9) was derived otherwise similarly to model set 6, but all possible interactions among the nest predation rate, mean spring temperature and flycatcher density were included in the global model (see Table S10 for the set of averaged models). | 8       LOUKOLA et al. Model sets 8 (Table S11; see Table S12, for the set of averaged models) and 9 (Table S13; see Table S14, for the set of averaged Model set 2 showed no evidence of any interactions among the hypothesized mechanisms affecting clutch coverage (Table 2b). models)) tested whether the clutch coverage of tits or the ecolog- When focusing only on sites where flycatchers are present ical and abiotic environment explain the number of fledged off- (model set 3), clutch coverage was positively associated with the spring of great tits and were derived otherwise similarly to model flycatcher density (Figure 3), but the mean spring temperature and sets 6 and 7, respectively, but number of fledged offspring was nest predation rate effects disappeared in this smaller subset of the used as a dependent variable. Population was set as a random ef- data (Table 3a). fect in all models. Model set 4 showed no evidence of any interactions among the Model set 10 (Table S15; see Table S16, for the set of averaged models) was otherwise similar to model set 1, but flycatcher density was replaced with flycatcher presence (binary variable; flycatcher present or not) for checking whether the results are sensitive to the way how flycatcher density is handled (continuous vs. presence/ absence). hypothesized mechanisms affecting clutch coverage on sites where flycatchers are present (Table 3b). Model set 5 showed that clutch coverage of blue tits was not associated with any of ecological or abiotic factors (Table S5). Model sets 6 and 8 showed that both the numbers of hatched eggs and fledged offspring were positively associated with clutch size, as expected, and number of fledged offspring was positively associated with mean spring temperature, but neither of them was 3 |   R E S U LT S associated with clutch coverage, predation rate, flycatcher density or female age (Tables S7 and S11 and Figures S2 and S3). Model set 1 showed that clutch coverage of great tits was negatively Model sets 7 and 9 showed no evidence of any interactions associated with the mean spring temperature, positively associated among the hypothesized mechanisms affecting reproductive suc- with nest predation rate and nest floor surface area (Table 2a and cess (Tables S9 and S13). Figure 2). Clutch coverage was also affected by the dominant tree Model set 10 showed that replacing the flycatcher density to genus, being particularly high at sites dominated by genus Citrus flycatcher presence as an explanatory variable did not change the trees (Table 2a). model-averaged results (Table S15). PC1 2 0 e verag tch co of clu 1 −1 10 ra t 14 16 pe of 20 ne sts ur e 12 pr 10 ed at Te m −2 Pe40 rc en 30 ta ge ed 0 18 F I G U R E 2   Regression surface illustrating the relationship between the mean spring temperature (°C), nest predation rate and clutch coverage (first principal component of proportion of clutch covered and mass of the cover material) in great tits. The surface was drawn by using model-averaged parameter estimates based on the assumption of additive effects of mean spring temperature, nest predation rate and flycatcher density (Table 2a) for nest predation rate and mean spring temperature effects, setting dominant tree genus to Betula and nest floor surface area to its mean value. Variables that, according to model averaging, did not explain clutch coverage were ignored F I G U R E 3   Clutch coverage of great tits in relation to flycatcher density (%) in populations where flycatchers were present. Circles depict data, and the line is a regression line based on modelaveraged parameter estimates for flycatcher density effect (Table 3a). Variables that, according to model averaging, did not explain clutch coverage were ignored. The same analysis was repeated without the observation with the highest flycatcher density (>80%). This did not qualitatively change the model-averaged results (see Table S17; see Table S18, for the set of averaged models and Figure S4) |       9 LOUKOLA et al. 4 | D I S CU S S I O N other competitors makes sense because the clutch size may provide accurate and reliable inadvertent information about the environment The aim of this study was to investigate large-scale geographical and the quality of the tit parents to prospecting birds. Environmental variation in great and blue tits' egg covering behaviour in Europe and variation explains a large amount of variance in clutch size (Beldal et al., variables that may explain egg covering behaviour. In particular, we 1998; Charmantier, Perrins, McCleery, & Sheldon, 2006; McCleery test three hypotheses, the insulation, nest predation and information et al., 2004; Tremblay et al., 2003) suggesting that clutch size reliably parasitism hypotheses, suggested to explain the egg covering behav- reflects the quality of the environment and can be readily used as a iour of tits. Our results from 28 different populations across Europe cue about territory quality. Moreover, the clutch size of tits may reveal show that the clutch coverage of great tits is more extensive with their competence in cognition and decision-making (Cauchard et al., lower mean spring temperature and higher nest predation rate. The 2017; Cole, Morand-Ferron, Hinks, & Quinn, 2012) and the pied fly- analysis also suggests that the increasing flycatcher density is asso- catchers have been shown to use clutch size of tits as a primary cue ciated with increased egg covering in great tits. However, this effect of whether to copy or reject observed tit choices, such as a novel nest was found only in populations where breeding flycatchers were pre- site feature preference (Loukola et al., 2013). By covering the eggs, tits sent. Despite flycatchers being absent from some study sites, they would hide this information from flycatchers. Without the information were breeding in the vicinity of most of these sites, which means about the tits’ success, flycatchers may reject the behaviour of the ob- that we may have only tit populations with co-evolutionary history served tits more frequently and may be less likely to settle in the im- with flycatchers in our data. The hypothesized mechanisms appear mediate neighbourhood of a tit nest. Flycatchers breeding close to tits to have additive effects on egg covering behaviour. Thus, these re- have a negative effect on tit offspring number and condition (Forsman sults support the mutually non-exclusive hypotheses that have been et al., 2007). Consistent with this, a recent study (Loukola et al., 2013) put forward to explain egg covering behaviour in great tits, suggest- suggested that flycatchers tended to reject the choices of ostensibly ing that egg covering may have multiple functions. In blue tits, clutch successful tits when the clutch was covered. This, in turn, may reduce coverage was not associated with any of ecological or abiotic fac- the costs of interspecific competition (Loukola et al., 2013). tors, but one should be careful in interpreting these results due to the limited sample size. Interspecific exploitation, or eavesdropping (Kroodsma & Miller, 1996) of inadvertent signals is important because it may affect the First, clutch coverage may provide thermal insulation against low evolution of extended phenotypes. Usually the evolution of bodily temperatures in spring during egg-laying, in a period when the fe- and non-bodily signals are assumed to result from conflicting selection males are not staying in the nest for long periods at a time during the pressures from natural and sexual selection (Schaedelin & Taborsky, day. This is in line with Haftorn and Slagsvold (1995), who found that 2009). For example, sexual selection may enhance the size and show- egg covering tended to be negatively related to the increasing am- iness of the nest (Mainwaring et al., 2014; Schaedelin & Taborsky, bient air temperature in great tits. Also, Loukola et al. (2014) found 2009) while natural selection is expected to reduce the size and the that, in Finland, great tits had 54.5% (0.5 g) more hair on the eggs in visibility of the nest due to nest predation (Biancucci & Martin, 2010). Oulu than in Turku. Oulu (latitude 65°) is located over 600 km north If information use by other species affects negatively or positively the of Turku (latitude 60°) and the mean daily spring temperature was performance of the species whose extended phenotype is used as a 2.4°C cooler (in years 1981–2010) in Oulu (Pirinen et al., 2012). source of information, it brings about coevolution as a potential mech- Second, egg covering behaviour might be a protection against nest anism affecting the evolution of extended phenotypes. In concert with predators. Yet, it seems unlikely that hair or feather cover could pre- other recent studies (e.g. Gotelli, Graves, & Rahbek, 2010; Mönkkönen, vent small predators such as weasel (Mustela nivalis) or stoat (Mustela Devictor, Forsman, Lehikoinen, & Elo, 2017), our results imply that erminea) from finding the eggs underneath the covering material. Tits local species interactions can reflect to biogeographical patterns and also cover eggs in the populations where mustelids are absent, for should also be considered jointly with abiotic factors, which often are example on Gotland, Sweden. However, it is possible that covering solely used to explain large-scale patterns. the eggs may cheat naive predators into believing that there are no Our results also showed that extent of egg covering increased eggs in the nest (Perrins, 1979). Also, predators such as woodpeckers with increasing nest floor surface area. This suggest that the eggs are (Picidae), that have small olfactory bulbs (Bang & Cobb, 1968), and spread out over a wider area in nest boxes with larger floor area and thus use mostly visual cues when searching for food, could perceive more material would be then needed to cover the eggs. Clutch cover- a nest with covered eggs as an empty nest. If egg covering prevents age was also affected by the dominant tree genus, being particularly even some of the nest predation attempts by any of the predators, high at site (Sagunto, east Spain) dominated by genus Citrus, where selection for egg covering could be expected. This is because the several nest competitors/predators (black rats [Rattus rattus], house nest predation is among the most important factors affecting the be- sparrows [Passer domesticus] and garden dormouse [Eliomys querci- haviour and life history traits in birds (Martin & Briskie, 2009). How nus]) occur in high numbers (Barba & Gil-Delgado, 1990; Gil-Delgado, egg covering affects the behaviour of different predators, remains to Tamarit, Viñals, Gómez, & Vives-Ferrándiz, 2009). However, leaving be tested. the data from Sagunto out from the model set 1 did not change the Third, egg covering could be a defence (counter-adaption) to reduce model-averaged results (Table S19; see Table S20, for the set of aver- information parasitism. Hiding the clutch size from flycatchers and aged models). One explanation for the differences in clutch coverage | 10       LOUKOLA et al. among study sites may have been variation in the availability of suit- of coevolution theory that predicts that interspecific interactions able covering materials. The density and the species composition of occur at the population scale and may result in different outcomes in local bird and mammal communities, which are linked to various char- different localities (Thompson, 2005). Therefore, geographical vari- acteristics of the habitat, including tree species, affect the availability ation in species co-occurrences should be taken into account when of feathers and hairs. The fact that not all tits cover their eggs suggests studying how interspecific interactions affect (co)evolution. that some costs are involved. These may include not only the costs of locating and bringing the materials to the nest but also the risk of AC K N OW L E D G E M E N T S adult predation when collecting. Egg covering materials (mammal hair, O.J.L. was funded by Biological Interactions Graduation School feathers) are usually found on the ground where the risk of predation (BIOINT), the Jenny and Antti Wihuri Foundation/the Foundation's on the female (only the female builds) may be high at a stage where Post Doc Pool and Academy of Finland grant no. 24302601. her body mass is high due to the production of eggs. Also, infestation J.C.S. was funded by CGL-2016-79568-C3-3-P research project risk by ticks (Ixodidae) is almost entirely limited to lower levels of the from the Spanish Research Council (Ministry of Economics and vegetation (Humair, Turrian, Aeschlimann, & Gern, 1993). Competitiveness). S.M.K. was funded by Academy of Finland (grants The reproductive success of great tits was not significantly associ- No. 314833 and 319898). J.T.F. was funded by Academy of Finland ated with clutch coverage. This suggests that egg covering had limited (grant no. 122665 and 125720) and Kone Foundation. The authors fitness consequences for the tits in the year of study. Year 2013 was declare that there is no conflict of interest. phenologically an extremely late year for nesting of forest passerines in most parts of Europe (Glądalski et al., 2016; Wesołowski, Cholewa, DATA AVA I L A B I L I T Y S TAT E M E N T Hebda, Maziarz, & Rowiński, 2016; F. Adriaensen, unpublished data) Data associated with this article are deposited in the Dryad Digital and it may have affected the reproductive investment decisions of Repository https://doi.org/10.5061/dryad.3bk3j9kft. tits in general. Long-term data and manipulative experiments, such as adding/removing covering of eggs or manipulation of temperature ORCID within nests (see e.g. Bleu, Agostini, & Biard, 2017) or nest predation Olli J. Loukola  https://orcid.org/0000-0002-9094-2004 risk perception (see e.g. Doligez & Clobert, 2003) could be the next Peter Adamik  https://orcid.org/0000-0003-1566-1234 step to test whether the egg covering behaviour is an adaptive trait. Emilio Barba  https://orcid.org/0000-0003-2882-9788 https://orcid.org/0000-0003-3015-5022 Blandine Doligez  5 |  CO N C LU S I O N Tapio Eeva  https://orcid.org/0000-0002-0395-1536 Sami M. Kivelä  https://orcid.org/0000-0002-6844-9168 Toni Laaksonen  https://orcid.org/0000-0001-9035-7131 Egg covering most likely serves multiple functions in great tits. It Chiara Morosinotto  provides thermal insulation against cold temperatures and hides Raivo Mänd  https://orcid.org/0000-0002-9172-894X the eggs from the nest predators looking for an egg meal and from Petri T. Niemelä  https://orcid.org/0000-0002-7518-4057 information parasites searching for clutch-size information. The Vladimir Remeš  https://orcid.org/0000-0001-8919-1496 interactions among the nest predators, information parasites and Jelmer M. Samplonius  tits are expected to result in a series of adaptations and counter- Manrico Sebastiano  https://orcid.org/0000-0002-0878-1775 adaptations, egg covering having a function in hiding the eggs. Juan Carlos Senar  Hence, our results suggest that interspecific interactions also shape Tore Slagsvold  extended nest phenotypes of birds, resulting in geographical vari- Barbara Tschirren  ation in nest characteristics, depending on the co-occurrence of János Török  interacting species. Social information use as a mechanism shaping Jukka T. Forsman  https://orcid.org/0000-0002-8700-4041 https://orcid.org/0000-0002-9186-0772 https://orcid.org/0000-0001-9955-3892 https://orcid.org/0000-0003-2410-3269 https://orcid.org/0000-0003-4806-4102 https://orcid.org/0000-0002-4799-5522 https://orcid.org/0000-0002-4156-7930 the extended phenotypes in general has gone unnoticed (Schaedelin & Taborsky, 2009) but is likely to be common in nature. Many ex- REFERENCES tended phenotypes are long-lasting and readily available for coexist- Bang, B. G., & Cobb, S. (1968). The size of the olfactory bulb in 108 species of birds. 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Immense plasticity of timing of breeding in a sedentary forest passerine, Poecile palustris. Journal of Avian Biology, 47(1), 129–133. https​//doi.org/10.1111/jav.00733​ : White, D. W., & Kennedy, E. D. (1997). Effect of egg covering and habitat on nest destruction by House Wrens. Condor, 873–879. https​//doi. : org/10.2307/1370137 B I O S K E TC H Olli J. Loukola is a post-doctoral researcher at University of Oulu, Finland. He is a behavioural ecologist and his research focuses on the information use within and among species and its ecological and evolutionary implications. Read more at: https​//www.resea​ : rchga​ e.net/profi​e/Olli_Loukola2 t l Author contributions: The experiment was designed by O.J.L. and J.T.F. Data were collected by O.J.L., P.A., F.A., E.B., B.D., E.F.J., T.E., T.L., C.M., R.M., V.R., J.M.S., M.S., J.C.S., B.T., J.T. and J.T.F. and analysed by O.J.L., S.M.K. and P.T.N., and all authors contributed to writing of the manuscript. All authors have read and approved the final manuscript. S U P P O R T I N G I N FO R M AT I O N Additional supporting information may be found online in the Supporting Information section.  How to cite this article: Loukola OJ, Adamik P, Adriaensen F, et al. The roles of temperature, nest predators and information parasites for geographical variation in egg covering behaviour of tits (Paridae). J Biogeogr. 2020;00:1–12. https​//doi.org/10.1111/jbi.13830​ :