Yiting Jiang ,Yujia Bi ,Ruiyao Ma,Jing Zhang,Dongmei Wan

Laboratory of Animal Resource and Epidemic Prevention,School of Life Sciences,Liaoning University,Shenyang,110036,China

Keywords:Cinereous Tit Conspeci fic nest distance Heterospeci fic nest distance Reproductive effect Varied Tit

ABSTRACT The spatial distribution and breeding behavior of neighboring birds(conspeci fic and heterospeci fic)may in fl uence reproduction and the effects differ across species.In this study,we investigated intra-and inter-speci fic spatial distribution of breeding via arti ficial nestboxes and examined whether overlap with neighbors affected reproductive success of the focal breeding pair.Regarding spatial distribution,Varied Tits(Sittiparus varius)and Cinereous Tits(Parus cinereus)showed similar pattern:distances of nestboxes containing conspeci fic tits were greater than those with heterospeci fic ones.In terms of breeding behavior,reproductive success was not significantly related to the distance from their neighbor’s nest.The reproductive success of Varied Tits was signi ficantly related to that of their neighbors,while in Cinereous Tits,no strong link was found to any recorded reproductive behavior of the neighbors.These findings explain spatial variation in nest site selection of Varied Tits and Cinereous Tits.Reproductive success rate of Varied Tits is affected by that of the neighbors while that of Cinereous Tits is not.The results highlight that there are differences in reproductive outcome among related species and offer suggestions on the use of arti ficial nestboxes in experiment and conservation programs.

1.Introduction

There often is competition for limited resources when species live in the same area,especially in the breeding season.Individuals need suitable nest sites(Martin,1993)and suf ficient food resources for survival and reproduction(Martin,1987).They also want to avoid losses caused by interference competition(Minot and Perrins,1986;review in Dhondt,2012).

A large number of experimental studies have shown that intra-and inter-speci fic competition can reduce breeding success and population size(Schoener,1983;Finch,1990;Gurevitch et al.,1992).House Wrens(Troglodytes aedon)that co-habit with Tree Swallows(Tachycineta bicolor)have lower reproductive success rate than wrens living in swallow-free plots(Finch,1990).The first egg laying date of Eurasian Blue Tits(Cyanistes caeruleus)is affected by intra-speci fic and inter-speci fic interference,but no such relationship has been found in a closely related species,the Great Tit(Parus major,Møller et al.,2018).The reproductive output of the central nest is adversely affected by their short-distance neighbors containing conspeci fics but not heterospeci fic ones(Deeming et al.,2017).Most studies have concentrated on the breeding behavior of conspeci fic or heterospeci fic neighbors to evaluate intra- and inter-speci fic competition.Breeding synchrony may also be an important environmental indicator as needs for resources vary hugely as nestlings grow.Competition might lead greater intervals among neighbors in terms of delay in breeding and might have effects on reproduction in neighbors.

Some species are suf ficiently abundant and show no obvious spatial heterogeneity,while others are range-restricted and in fl uenced by both habitat composition and local environment(Laube,2011).Regarding the question of what affects the size of the distribution,most studies concentrated on non-behavioral environmental or spatial factors(e.g.Szabo et al.,2009;Boucher-Lalonde et al.,2014)but few have investigated behaviors.Zhang et al.(2019)attributed the difference in the distribution size of Cinereous(Parus cinereus)and Varied Tits(Sittiparus varius)to their personalities because the relatively wider-spread Cinereous Tit is more exploratory,active,and risk-prone than the Varied Tit,a locally distributed species,is.We predict that anti-interference capability of the narrowly-distributed Varied Tit may be weaker than that of the relatively widely-distributed Cinereous Tit.

Arti ficial nestboxes are widely used in studies of birds,particularly in field research,because they attract breeding birds.As a result,it is an effective tool to gather reproduction data(Møller et al.,2014)to study demographic shift,life history evolution,quantitative genetics,and sexual selection(Evans et al.,2002).To ensure suf ficiency,usually large numbers of arti ficial nestboxes are provided,but only a small number are occupied every year(M¨and et al.,2005).

In this study,we measured intra-and inter-speci fic spatial distribution of used arti ficial nestboxes and investigated whether the intersection of neighbors’living area affected the breeding outcome of the focal breeding pair.Two hole-nesting passerine species,Cinereous Tit and Varied Tit,were concentrated on.Based on which we proposed three hypotheses:(1)the distance of nests within species is longer than that between them,(2)conspeci fic and heterospeci fic neighbors both have a negative impact on the focal nest,and(3)the range-restricted species,Varied Tits,are more vulnerable to neighbor in fl uence than the relatively wider-spread Cinereous Tits.

2.Materials and methods

2.1.Study area and data collection

Starting from 2016,this study was carried out every year from early April through mid-July for three consecutive years in Liaoning Xianrendong National Nature Reserve(39°54ʹ‒40°03ʹN,122°53ʹ‒123°03ʹE).Yet ten years before this study began arti ficial nestboxes had already been installed and supplemented or replaced every year.All boxes had a base dimension of 15 cm×15 cm and a height of 30 cm.The opening was round,with a diameter of 3 cm or 3.5 cm,and located about 7 cm below the box cover.The arti ficial nestboxes were hung mainly on Pinus densi fl ora,Quercus mongolica and Pinus koraiensis,at a height of 2–3 m from the ground.

All boxes were hung randomly on both sides along infrequent paths in the reserve.Their locations were recorded using OvitalMap(Beijing Ovital Software Co.Ltd.2016).The average distance between two nearest ones was around 30 m.Weekly recording included the laying date,the species(available since incubation)and reproductive parameters such as clutch size,the number of hatchlings,ten-day-old nestlings and fl edglings.We then calculated the hatching rate(the number of hatchlings/clutch size)and reproductive success rate(the number of fl edglings/clutch size).The distances from the central nestbox to(1)the nearest ones,(2)the nearest nestbox occupied by a conspeci fic,and(3)the nearest nestbox occupied by a heterospeci fic were all measured using OvitalMap.

2.2.Statistical analyses

The data was analyzed in SPSS version 21.0(IBMCorp.Armonk,NY).An index of dispersion(Fowler et al.,1997)was calculated to ascertain the box distribution pattern.Mixed effect regression was used to test factors(the explanatory variable:neighbor type;and the random factors:box number and year)that affected the intra-and inter-speci fic nest spacing(the response variables:the distance between the focal nest and its nearest conspeci fic/heterospeci fic nest).We used mixed effect models to explore the in fl uence of spatial distribution on the hatching rate of the focal nest(the explanatory variables:conspeci fic distance,heterospeci fic distance;and the random factors:box number and year)and linear models to explore the in fl uence of spatial distribution on the reproductive success rate of the focal nest(the explanatory variables:conspeci fic distance,heterospeci fic distance).We used mixed effect models to explore the in fl uence of breeding behavior on the hatching rate of the focal nest(the explanatory variables:neighbor type,neighbor hatching rate,and breeding synchrony;and the random factors:box number and year)and linear models to explore the in fl uence of breeding behavior on the reproductive success rate of the focal nest(the explanatory variables:neighbor type,neighbor reproductive success rate and breeding synchrony).All analyses were considered signi ficant at a probability value of<0.05.

3.Results

In total,340,451 and 434 nestboxes were investigated in 2016,2017 and 2018,respectively.Each year less than half were occupied(Table 1)mainly by Cinereous Tits and Varied Tits,while few were occupied by other species such as Marsh Tits(Poecile palustris)and Daurian Redstarts(Phoenicurus auroreus).Over the 3 years,20 boxes were used twice by Cinereous Tits,17 boxes were used twice by Varied Tits,and 1 box was used thrice by each.All boxes were randomly dispersed within 500 m on both sides of the path(e.g.,Fig.1,dispersion indicesχ2=13.46,df=19),as were those occupied by both Varied Tits(χ2=8.68,df=19)and Cinereous Tits(χ2=18.02,df=19).

The distance between breeding nests was signi ficantly affected by neighbor type(F=29.652,P<0.001),but not species(F=1.304,P=0.254).The distance between intraspeci fic breeding nests of Varied Tits was signi ficantly longer than that between interspeci fic nests(Fig.2A).For Cinereous Tits,the same was true(Fig.2B).However,reproduction of Varied and Cinereous Tits was not signi ficantly relevant to the distance from their neighbor’s nest(Table 2).

Table 1 The total number of nestboxes placed,occupied and the occupancy rate in 2016,2017,and 2018.The main species that used the arti f icial nestbox were Varied Tit and Cinereous Tit.

Table 2 Statistical results of the effect of conspeci fic and heterospeci fic neighboring nest distance on the focal nest’s hatching rate(mixed effect models)and reproductive success(linear models).The mixed effect model for the Cinereous Tit had the statistics n=70,r2=0.055,and for the Varied Tit n=72,r2=0.026.The linear model for the Cinereous Tit had the statistics n=53,F2,14=0.121,r2=0.017,and for the Varied Tit n=53,F2,16=0.282,r2=0.034.

The hatching rate of Varied Tits(n=144,r2=0.892)was not related to recorded breeding behavior of their neighbors(hatching rate,t=0.773,P=0.982;and breeding synchrony,t=-0.419,P=0.333).Its reproductive success rate(n=38,r2=0.270,F5,32=2.362,P=0.062)was negatively related to that of their neighbors(t=-2.677,P=0.012)and positively related to the interaction between neighbor type and the reproductive success rate of the neighbor(t=2.142,P=0.040).Separate analyses on intraspeci fic neighbor and interspeci fic neighbor showed that the reproductive success of Varied Tits was negatively related to that of intraspeci fic neighbor(t=-2.889,P=0.011,Fig.3)and not significantly related to that of interspeci fic neighbor(t=-0.086,P=0.932,Fig.3).The reproductive effect of Cinereous Tits(hatching rate,n=140,r2=0.758;and reproductive success rate,n=34,r2=0.201,F5,28=1.404,P=0.253)was not signi ficantly affected by the recorded breeding behavior of their neighbors.

4.Discussion

There was spatially separated nest sites selection for Varied Tits and Cinereous Tits.The distance between nests was longer within than between species.While both inter-and intra-speci fic competitions affect site selection(Tarjuelo et al.,2017)and food abundance(Teather,1992),intraspeci fic competition in particular also impacts mate choice(Martínez-Rivera and Gerhardt,2008)and extra-pair mating(Birkhead et al.,1985).To reduce such competition,individuals of the same species may space each other's nesting sites farther apart.Thus,intra-speci fic nests were more sparsely spaced.Deeming(2017)also shows that the conspeci fic nest distance is longer than the heterospeci fic one for Blue Tits and Great Tits.These results support that intraspeci fic competition in nest selection is more intense than interspeci fic competition.

Regarding spatial distribution,Varied and Cinereous Tits showed a similar pattern.The distance to their neighbor’s nest was not signi ficantly relevant to reproduction.But intense competition arises from the relatively short distance between two nests of the same species,which may adversely affect the reproduction of the breeding nest(Deeming et al.,2017).In our study,fewer than half of the installed boxes were occupied.The average distance between two nearest nestboxes was around 30 m,about twice the distance between two nearest neighbors.The space interval was relatively suf ficient,and that was not so drastic to affect the reproductive success.

The breeding success of Varied Tits may or may not be affected by that of their neighbors.The type matters.Between conspeci fic neighbors there is a negative correlation whereas between heterospeci fic ones,no identi fiable correlation.Competition can reduce the number of offsprings(Gurevitch et al.,1992).In resource-restricted habitat,we are likely to detect the effect of density-dependence on reproduction in territorial species(Dhondt,2010).When the conspeci fics reproduce in the same area,there will be severe competition for food(Krüger et al.,2012).Food shortage is known to disrupt reproduction.

Fig.1.Maps of Liaoning Xianrendong National Nature Reserve showing the distribution of the nestboxes.Solid black lines suggest the range on both sides of the paths.Circles indicate position of nestboxes in 2018 and the species occupying them.

Fig.2.Using mixed effect models to test the relationship between box distance and neighbor type(conspeci f ic/heterspeci f ic),box number and year.(A)Mean distance between the focal nest of Varied Tit(Sittiparus varius)and its conspeci f ic and heterospeci f ic neighbors.The distance between intraspeci f ic breeding nests(116.28±72.5 m,n=140)was signi f icantly longer than that between interspeci f ic nests(87.17±68.78 m,t=-3.537,P=0.001).The mixed effect model had the statistics F3,311=6.419,r2=0.059,P<0.001.(B)Mean distance between the focal nest of Cinereous Tit(Parus cinereus)and its conspeci f ic and heterospeci f ic neighbors.The distance between intraspeci f ic nests(108.40±71.04 m,n=155)was signi f icantly longer than that between interspeci f ic nests(79.80±55.50 m,t=-4.108,P<0.001).The mixed effect model had the statistics F3,311=5.769,r2=0.053,P<0.001.

However,Cinereous Tits did not show signi ficant correlation to any recorded reproductive behavior of their neighbors.The results are supported by Møller’s(2018)finding that the breeding behavior of Blue Tits is affected by conspeci fics but not Great Tits.In other words,the effect of competition on demographic variables has interspeci fic divergence.This may result fromthe either the scramble or exploitation-type competition for food both within and between species,and interference competition between different body sizes(Dhondt,1977,2010),as Cinereous Tits are larger than Varied Tits.Interspeci fic divergence may be related to the variances in clutch size of the two species.In our research site,the clutch size of Varied Tits is mostly 7–9,and the clutch size of Cinereous Tits is 7–13.Flexible adjustment of clutch size might be one of the ways for big tits to reduce competition.Behavioral differences may also contribute to the divergence.Active individuals can get more food resources under the same circumstance(David et al.,2011).So Varied Tits,which are less exploratory,active,and risk-taking than Cinereous Tits(Zhang et al.,2019),get less.Reproductive success of Cinereus Tits is not signi ficantly affected.

This study focused on one option of breeding site,namely through arti ficial nestboxes,rather than exhausting all possibilities.For example,nests in natural cavities are not considered.This is because on the reserve,where dead wood is removed in a timely manner,natural cavities are in insuf ficient supply.Before the breeding season,in March,we ringed the birds on the experimental site.During the entire breeding test period,unringed individuals were rarely spotted.Therefore,we assume that,at least in the area where arti ficial nest boxes were hung,natural nests were negligible.

Boxes that are too densely distributed can even negatively affect the breeding behavior of birds,especially in areas where natural nests are extremely scarce.Thus,arti ficial nestboxes usually have low occupancy rate(M¨and et al.,2005;Deeming et al.,2017).This knowledge can be applied to the arrangement of nestboxes for bird study and conservation.

Fig.3.Using linear regression to test the relationship between the reproductive success of the Varied Tit and that of its intraspeci fic neighbor(Varied Tit)and interspeci fic neighbor(Cinereous Tit),respectively.The reproductive success of the Varied Tits decreased with increasing reproductive success of intraspeci fic neighbor(t=-2.889,P=0.011)and was not signi ficantly related to that of interspeci fic neighbor(t=-0.086,P=0.932).The blue and red spots represented intra-and inter-speci fic neighbors.The solid lines were the linear regression lines.

5.Conclusions

Our results show that intra-and inter-speci fic competition affects the nest distribution of two hole-nesting species.The effect on reproductive outcome has interspeci fic divergence.The reproductive outcome of Varied Tits is signi ficantly affected by its conspeci fic and heterospeci fic neighbors,but that of Cinereous Tits is not affected.

Authors’contributions

YJ conceived the experiments,analyzed the data,wrote the manuscript,and reviewed the drafts;YB conceived and designed the experiments,performed the experiments,analyzed the data,and wrote the manuscript;RM analyzed the data;JZ performed the experiments;DW conceived and designed the experiments,and reviewed drafts of the paper.All authors read and approved the final manuscript.

Ethics statement

All our study procedures were approved by Liaoning Xianrendong National Nature Reserve.

Declaration of competing interest

The authors declare that they have no competing interests.

Acknowledgments

Thanks for the support of Liaoning Xianrendong National Nature Reserve.This work was supported by the National Natural Science Foundation of China(No.31872231 to DW,No.32000316 to YJ).