Biol Invasions DOI 10.1007/s10530-015-0952-x ORIGINAL PAPER The empty temporal niche: breeding phenology differs between coexisting native and invasive birds Ana Sanz-Aguilar . Martina Carrete . Pim Edelaar . Jaime Potti . Jose´ L. Tella Received: 4 February 2015 / Accepted: 1 August 2015 Ó Springer International Publishing Switzerland 2015 Abstract Invasive species face new environmental new habitats by making use of ecological opportunities, conditions in their areas of introduction. A correct e.g. empty temporal Eltonian niches. Specifically, they timing of reproduction is crucial for the successful may achieve this via conservatism of their native adjustment of individuals to their environments, yet reproductive phenology and/or via plasticity in their the temporal aspects of the niche are a neglected reproductive timing. Here we compare the reproduc- subject in the study of biological invasions. When tive phenology of a marshland passerine community introduced, exotic species could successfully invade composed of five successfully established tropical exotic species and twelve coexisting Mediterranean native species along four consecutive years. Both groups showed large differences in their phenology, with exotics reproducing along more months and later in the year than natives. One exotic species even & A. Sanz-Aguilar ( ) Á M. Carrete Á P. Edelaar Á breeds only in late summer and early autumn, when J. Potti Á J. L. Tella Estacio´n Biolo´gica de Don˜ana (CSIC), Ame´rico virtually all natives have ceased breeding and when Vespucio s/n, 41092 Seville, Spain overall bird abundance as well as primary production e-mail: [email protected] in cultivated areas (rice fields) were highest. Nonethe- M. Carrete less, estimates of population sizes and juvenile e-mail: [email protected] survival rates in the study area suggest that late P. Edelaar breeding is not maladaptive but instead highly e-mail: [email protected] successful. The striking difference in reproductive J. Potti timing suggests that the exotics may be taking e-mail: [email protected] advantage of a vacant Eltonian temporal niche, J. L. Tella possibly generated by high resource availability in e-mail: [email protected] human-transformed habitats (rice fields and other croplands) in the study area. This study highlights A. Sanz-Aguilar Instituto Mediterra´neo de Estudios Avanzados, IMEDEA the need to also consider the temporal aspects of the (CSIC-UIB), Miquel Marque´s 21, 07190 Esporles, niche when studying invasions. Islas Baleares, Spain Keywords Timing of reproduction Á Temporal M. Carrete Á P. Edelaar Universidad Pablo de Olavide, Ctra Utrera km 1, niche Á Biological invasions Á Grinnellian and Eltonian 41013 Seville, Spain niche Á Niche conservatism Á Weaver 123 A. Sanz-Aguilar et al. Introduction species tend to maintain their former reproductive timing (conservatism) whereas others completely The adjustment of species to new environments is a change their breeding time (plasticity) (Baker and central topic in ecology, evolution and conservation Ranson 1938). As examples of change, House spar- biology (Parmesan 2006; Williams 2008). Exotic rows, Passer domesticus, reproduced continuously species provide unique opportunities to assess how during establishment in North America and New species face novel biotic and abiotic conditions and Zealand whereas native European sparrows breed shift or conserve their niches (Sax et al. 2005; seasonally (Hengeveld 1994). At the population level, Lockwood et al. 2007; Blackburn et al. 2009; Larson Rufous-collared Sparrows, Zonotrichia capensis, et al. 2010). Two niche components have been clearly changed from continuous breeding in their native recognized: Grinnellian niches describe the species’ populations in Colombia to seasonal breeding (up to responses to the non-interacting environmental vari- autumn) in an introduced population in the USA ables (e.g. climate) that influence their large-scale (Miller 1965); and several passerines introduced in geographical distribution; and Eltonian niches New Zealand have increased the length of their describe the functional role and biotic interactions of breeding season relative to the United Kingdom species (Sobero´n 2007). (Evans et al. 2005). However, the role of phenology When exotic species are confronted with novel when studying Eltonian niche overlap (including environments to which they need to adjust, they may niche conservatism and niche expansion) mediated either keep their niche (niche conservatism) or they via resource competition has been poorly explored in may change it (i.e. niche plasticity), and that is true for animal invasion biology. both the Grinnellian and Eltonian niche. Recent Here we compare the reproductive timing of an studies have highlighted that many invasive species entire community of established exotic birds of conserve their Grinnellian niche in their invaded tropical origin with that of the native, temperate bird ranges (Wiens et al. 2010; Strubbe et al. 2013), so that community using the same habitats, and explore the Grinnellian niche conservatism has been recognized importance of this temporal niche axis for establish- as the most likely scenario for most bird invaders in ment success. The timing of reproduction is one of the Europe (Strubbe et al. 2013). However, Sol et al. major life history traits involved in the adaptation of (2002) suggested that behavioural flexibility can be birds to their environments (Lack 1968; Murton and important by providing individuals with the ability to Westwood 1977). Birds show dramatic seasonal expand or change their foraging habits and success- reorganizations in physiology (e.g. gonadal develop- fully invade novel environments, representing a ment), behaviour (e.g. song, courtship) and morphol- change in Eltonian niches. On the other hand, the ogy (e.g. plumage) linked to reproduction (Murton and opposite result (Eltonian niche conservatism and Westwood 1977). Photoperiodic signal is the main Grinnellian niche shift) has been found in an invasive driver regulating the timing of reproduction in birds arthropod, the signal crayfish Pacifastacus leniusculus (Dawson et al. 2001; Hahn and MacDougall-Shack- (Larson et al. 2010), so more studies are called for. leton 2008), although circannual programming is also Studies on plants have pointed out the importance known to be important (Helm et al. 2009; Visser et al. of differences in the temporal segregation of the niches 2010). As individuals should reproduce at the right of species to understand some successful invasions time to maximize their fitness (Martin 1987; Daan (Wolkovich and Cleland 2010), for example because et al. 1988; Thomas et al. 2001; Sanz et al. 2003), separation in time reduces (competitive) interaction. typically when food availability is maximal, addi- For other organisms, such as birds, the timing of tional cues such as temperature, rainfall, or social reproduction of exotic species in their novel environ- factors can fine-tune the timing of reproduction to ments has been a topic of some historic interest (Baker local conditions (Hahn et al. 1997; Ball and Ketterson and Ranson 1938). To maintain viable populations, 2008; Hau et al. 2008). Thus, differences in timing of exotic birds must rapidly adjust to novel environmen- reproduction are common between and within species tal conditions (e.g. climate, photoperiod, resources (Hahn et al. 1997), showing typical geographical and/or competitors; Blackburn et al. 2009) in the areas patterns. For example, in temperate zones, seasonal of introduction. When introduced, some individuals/ changes in the environment are highly predictable and 123 The empty temporal niche most temperate birds breed in spring and early conditions that would presumably maximize food summer, coinciding with the peak of food availability availability and fitness (i.e. invaders are selected to be (Cramp and Simmons 1977). In many of those similar to natives), or (2) whether they may avoid temperate habitats, early breeding is theoretically competition with natives in temperate areas by advantageous because of the higher renesting possi- utilizing ecological opportunities occurring at differ- bilities and also because fledgling survival and ent times of the year (i.e. invaders are selected to be recruitment generally decline with the progression of different from natives). Secondarily, by comparing the the breeding season (Lack 1968; Daan et al. 1988; reproductive timing of the tropical invaders in their Price et al. 1998; but see Penteriani et al. 2014). On the novel temperate range with that in their native tropical contrary, postponing reproduction should be disad- ranges we explore whether these matches or changes vantageous if this entails competition for food with in reproductive timing are due to niche flexibility (as migrant or wintering individuals or if ecosystem might be predicted by the greater flexibility and production (i.e. food resources) decreases with the variation in reproductive timing in tropical birds, Hau advancing of the season, potentially leading to partial et al. 2008), or by niche conservatism (Strubbe et al. or total reproductive failure. In contrast, related to the 2013). In order to answer these questions we compared less seasonal climate, tropical birds show a wider the timing of reproduction of a successfully estab- range of breeding strategies, from seasonal to oppor- lished and spreading community of exotic passerines tunistic and continuous breeding (Hau et al. 2008). In in southern Spain (Sanz-Aguilar