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the dynamics of bird populations are influenced by climate change on both regional and local scales ( crick and sparks 1999 ; hallett et al .
there is good evidence from europe and north america that many avian species nowadays migrate and breed earlier as a result of higher temperatures ( crick 1997 ; tryjanowski et al .
2002 ; huppop and huppop 2003 ; parmesan 2007 ; bauer et al . 2010 ; matthysen et al .
the impact of the changes varies for different latitude , longitude , topography , etc .
, global warming not only means higher temperatures but also more frequent extreme weather events ( ogi et al .
2010 ; wu et al . 2012 ; zhang et al . 2012 ; coumou and rahmstorf 2012 ; tang et al . 2013 ) . in light of many recent extreme events all over the globe in 2012 and 2013 ( peterson et al . 2013 ; vaughan et al . 2013 ; zscheischler et al . 2013 ; some of which are considered to be the result of climate change ) , there is a possibility that distinctly low temperatures in the early spring 2013 could probably be linked to climate change . on the other hand , some climatologists think that there is no link between recent extreme events and climate change ( wallace et al .
2014 ) , but regardless of what is the reason for the extreme spring 2013 at our area and assuming that there is a potential for more frequent occurrence of atypical years , in the course of climate changes , we should study extreme weather phenomena and their consequences for wild populations . in 2013 ,
march 2013 was the coldest in the uk meteorological records since 1962 ( measurement since 1910 ; slingo 2013 ) , and in central europe , the temperatures were also much below recent averages , and as a result , many temperature records were beaten ( andrews 2013 ; harris 2013 ) . because of unusually low late winter / early spring temperatures , for many european countries , march 2013 was the snowiest march in at least 400  years ( harris 2013 ) .
in central poland , snow cover was still almost complete until 9 april in urban parks and until 15 april in forests ( gldalski , personal observation ) . according to some researchers ,
the basic cause of those extreme weather phenomena could be the melting of arctic ice cap , which caused a long - lasting inflow of cold air to europe ( li et al .
some authors think that there may be existing connection between arctic sea ice loss caused by global warming and large - scale circulation patterns in the northern hemisphere ( francis et al .
2009 ; francis and vavrus 2012 ; jaiser et al . 2012 ; screen et al . 2013
( 2013 ) conclude that there is a need to collect long - term phenology monitoring data in order to fully understand the impacts of climate change on different species .
( 2010 ) note in addition that , surprisingly , most papers analysing these trends do not use data from central europe , and there is a need to fill this gap .
the aim of this paper is to show the influence of an extreme weather event in spring 2013 ( unique over at least 40  years ) on the timing of breeding of great tits ( parus major ) and blue tits ( cyanistes caeruleus ) by comparison with the data from the preceding decade .
this study was carried out in 19992013 as part of a long - term project of research into the breeding biology of hole - nesting birds occupying nest boxes near d ( 51 47 n , 19 28 e , central poland ) .
study areas are located in two , 10-km - distant , structurally and floristically contrasting types of habitats : an urban parkland and a rich deciduous forest .
data analysed include tit breeding seasons ( april  may ) 19992013 in the parkland and 20022013 in the forest ( marciniak et al . 2007 ; kaliski et al . 2012 ) .
2010 ) , c. 200 in the parkland area and c. 300 in the forest . in spring , all nest boxes were checked for first egg dates and other breeding characteristics of tits .
a total of 1,182 first clutches of great tit ( 735 from the parkland and 447 from the forest ) and 861 first clutches of blue tit ( 412 from parkland and 449 from the forest ) were studied between 1999 and 2013 .
following perrins and mccleery ( 1989 ) , we calculated warmth sums , as the sum of the maximum daily temperatures for the period between 15 march and 15 april each year , to characterise thermal conditions .
we used cook s distance to measure how extreme 2013 was in comparison with the trend for 14 preceding years ( being the background for our phenological data on tits ) .
in addition , in order to compare the 15 march15 april warmth sum for 2013 with the warmth sums for a longer period encompassing 40  years of available records ( 19732012 ) , we used a special version of t test described by sokal and rohlf ( 1994 ) .
we used one - way anova followed by dunnett s post hoc test to compare mean laying dates between years .
graphical and statistical analyses were conducted applying statistica 6 ( statsoft , inc . , 2003 ) .
the warmth sum was extremely low in 2013 in comparison with the values for the preceding 14  years ( fig .  1 ) . when we excluded 2013 , there was a trend for warmth sums to increase during 19992012 ( r  =  0.53 , n  =  14 ,
the mean warmth sum for the period 19992012 was 338.5  c , increasing by 2.34  c per year ( the mean for 20022012 was 347.8  c ) , compared to 90.2  c in 2013 .
the cook s distance for the 2013 data point in temporal trend line shows that this point is a very strong outlier ( 4.62 ) , whereas the median distance ( 19992013 ) is 0.03 , while the second highest distance in the analysed period is only 0.14 ( 2012 ) ( fig .  1 ) .
when the data point for 2013 is included into the regression , the relationship between the warmth sum and years becomes nonsignificantly negative .
the 15 march15 april warmth sum for 2013 is extremely low also in a wider comparison with the warmth sums for the preceding 40  years .
the value for 2013 is below the lowest marginal warmth sum in 19732012 ( ranging from 185.5 to 436  c ; mean 315.1  c    64.3 sd ) , resulting in a highly significant difference ( t  =  3.46 , df  =  39 , p  <  0.001).fig .
1warmth sums ( sums of the daily maximum temperatures between 15 march and 15 april ) by year for the period 19992013 , including temporal trend line ( excluding 2013 ) warmth sums ( sums of the daily maximum temperatures between 15 march and 15 april ) by year for the period 19992013 , including temporal trend line ( excluding 2013 ) the yearly mean date of first egg laying was highly negatively correlated with the warmth sums over the study years at both study sites for both tit species : for great tits , r  =  0.79 , n  =  15 , p  <  0.001 in the parkland ( 19992013 ) and r  =  0.81 , n  =  12 , p  =  0.002 in the forest ( 20022013 ) , and for blue tits , r  =  0.77 , n  =  15 , p  <  0.001 in the parkland ( 19992013 ) and r  =  0.85 , n  =  12 , p  <  0.001 in the forest ( 20022013 ) . at both study sites , the mean laying dates each year in the period 19992012 ( parkland ) and 20022012 ( forest ) are earlier than in 2013 ( anova : for the great tit in the parkland , f14,721  =  38.95 , p  <  0.001 , and in the woodland , f11,436  =  48.20 , p  <  0.001 , and for the blue tit in the parkland , f14,397  =  19.48 , p  <  0.001 , and in the woodland , f11,437  =  44.09 , p  < 
0.001 ) ( figs .  2 and 3 ) . all differences between 2013 and the preceding years were significant for both species , except for blue tits in parklands in 2003 and 2006 ( post hoc dunnett s tests )
2mean laying dates ( days from 1 march ) of great tits and blue tits in 19992012 vs. 2013 in the parkland site . mean laying dates are presented as averages    95  % standard error intervalsfig .
3mean laying dates ( days from 1 march ) of great tits and blue tits in 20022012 vs. 2013 in the forest site .
mean laying dates are presented as averages    95  % standard error intervals mean laying dates ( days from 1 march ) of great tits and blue tits in 19992012 vs. 2013 in the parkland site .
mean laying dates are presented as averages    95  % standard error intervals mean laying dates ( days from 1 march ) of great tits and blue tits in 20022012 vs. 2013 in the forest site .
mean laying dates are presented as averages    95  % standard error intervals
mean dates of first egg laying by great tits and blue tits were highly correlated with spring ( pre - laying ) thermal conditions ( in our region , the period between 15 march and 15 april is crucial ; gldalski 2013 ) , with earlier laying occurring in warmer years . the temperature trend ( 19992012 ) ,
yet , the 15 march and 15 april warmth sum in 2013 was lower than that in any spring during 19732012 . in 2013 , the beginning of spring was extremely cold , and therefore , initiation of breeding was significantly delayed .
some delays in the timing of breeding were also found for both tit species in 2003 and 2006 . although the spring warmth sums in 2003 and 2006 were not distinctly low , the preceding winters were relatively severe , with the long - lasting snow cover and some adverse weather spells occurring even in early april , which could prevent females from early laying ( gldalski 2013 ) . currently , many avian species in europe migrate and breed earlier as a result of higher temperatures caused by global climate changes ( crick and sparks 1999 ; tryjanowski et al .
2002 ; both et al . 2004 ; both and visser 2005 ; parmesan 2007 ; matthysen et al .
the great tit and the blue tit are among such earlier breeding species ( potti 2009 ; bauer et al .
however , the force of impact of climate warming on reproductive parameters of both tit species seems to vary depending on variables such as longitude , latitude , topography , orientation of slopes , etc . , and as a result , in some areas , it may be too weak to be detectable ( sanz 2002 ) .
the effect is stronger for the populations of birds in western europe ( including mediterranean area ) , where warmer and wetter winters in recent times result in accelerated breeding .
the effect in eastern europe is weaker  it has a less distinct influence on fewer species ( sanz 2002 ; visser et al .
our study shows that extreme phenomena may act in opposition to trends , but more data are needed , as 1  year is certainly not enough to draw too far - reaching conclusions .
therefore , extreme weather phenomena that influence wild avian populations should be recorded , especially because there is a potential for more frequent occurrence of atypical years associated with climate change .
it was extensively debated whether or not different species would be able to adapt quickly enough to keep up with gradually changing environment ( visser 2008 ) , but little attention was devoted to potential consequences of extreme weather events occurring more often .
2012 ) , and it will have consequences for life histories of different organisms ( robinson et al .
probably more extreme weather events and strong deviations from long - term trends , being very strong but unpredictable factors , could disturb life history strategies of some species and make it more difficult for organisms to adapt to local environments ( visser 2008 ; chamberlain and pearce - higgins 2013 ; fletcher et al . 2013 ) .
maybe this one outlier does not make a wider story by itself , but if similar outliers will appear more frequently , as there is potential for more atypical years as the result of climate change , then further investigations should focus on the impact of extreme events on different life history traits , such as clutch size , hatching rate , reproductive success and proportions of second clutches .
the impact of climatic changes on life cycles by re - scheduling the timing of reproduction is an important topic in studies of biodiversity . global warming causes and 
 will probably cause in the future not only raising temperatures but also an increasing frequency of extreme weather events . in 2013 , the winter in central and north europe ended late , with low temperatures and long - retained snow cover  this extreme weather phenomenon acted in opposition to the increasing temperature trend . in 2013 , 
 thermal conditions measured by the warmth sum in the period 15 march15 april , a critical time for early breeding passerines , went far beyond the range of the warmth sums for at least 40 preceding years . 
 regardless of what was the reason for the extreme early spring 2013 and assuming that there is a potential for more atypical years because of climate change , we should look closely at every extreme phenomenon and its consequences for the phenology of organisms . in this paper , 
 we report that the prolonged occurrence of winter conditions during the time that is crucial for blue tit ( cyanistes caeruleus ) and great tit ( parus major ) reproduction caused a substantial delay in the onset of egg laying in comparison with typical springs .