1 The empty temporal niche: breeding phenology differs between coexisting native 2 and invasive birds 3 4 Ana Sanz-Aguilar1,2*, Martina Carrete1,3, Pim Edelaar1,3, Jaime Potti1 & José L. 5 Tella1 6 7 8 1Estación Biológica de Doñana (CSIC), Américo Vespucio s/n, E-41092 Sevilla, Spain 9 2 Instituto Mediterráneo de Estudios Avanzados, IMEDEA (CSIC-UIB), Miquel 10 Marqués 21, E-07190 Esporles, Islas Baleares, Spain 11 3Universidad Pablo de Olavide, Ctra Utrera km 1, E-41013 Sevilla, Spain 12 13 14 *Corresponding Author: Ana Sanz-Aguilar, Estación Biológica de Doñana (CSIC), 15 Américo Vespucio s/n, E-41092 Sevilla, Spain, Telephone: (+34) 954 232 340, Fax: 16 (+34) 954 621 125, E-mail: [email protected] 17 18 Authors e-mails: [email protected], [email protected], [email protected], 19 [email protected]; [email protected] 20 21 1 22 ABSTRACT 23 Invasive species face new environmental conditions in their areas of introduction. A 24 correct timing of reproduction is crucial for the successful adjustment of individuals to 25 their environments, yet the temporal aspects of the niche are a neglected subject in the 26 study of biological invasions. When introduced, exotic species could successfully 27 invade new habitats by making use of ecological opportunities, e.g. empty temporal 28 Eltonian niches. Specifically, they may achieve this via conservatism of their native 29 reproductive phenology and/or via plasticity in their reproductive timing. Here we 30 compare the reproductive phenology of a marshland passerine community composed of 31 five successfully established tropical exotic species and twelve coexisting 32 Mediterranean native species along four consecutive years. Both groups showed large 33 differences in their phenology, with exotics reproducing along more months and later in 34 the year than natives. One exotic species even breeds only in late summer and early 35 autumn, when virtually all natives have ceased breeding and when overall bird 36 abundance as well as primary production in cultivated areas (rice fields) were highest. 37 Nonetheless, estimates of population sizes and juvenile survival rates in the study area 38 suggest that late breeding is not maladaptive but instead highly successful. The striking 39 difference in reproductive timing suggests that the exotics may be taking advantage of a 40 vacant Eltonian temporal niche, possibly generated by high resource availability in 41 human-transformed habitats (rice fields and other croplands) in the study area. This 42 study highlights the need to also consider the temporal aspects of the niche when 43 studying invasions. 44 45 Keywords: timing of reproduction, temporal niche, biological invasions, Grinnellian and 46 Eltonian niche, niche conservatism, weaver. 2 47 INTRODUCTION 48 The adjustment of species to new environments is a central topic in ecology, evolution 49 and conservation biology (Parmesan 2006; Williams 2008). Exotic species provide 50 unique opportunities to assess how species face novel biotic and abiotic conditions and 51 shift or conserve their niches (Sax et al. 2005; Lockwood et al. 2007; Blackburn et al. 52 2009; Larson et al. 2010). Two niche components have been clearly recognized: 53 Grinnellian niches describe the species’ responses to the non-interacting environmental 54 variables (e.g. climate) that influence their large-scale geographical distribution; and 55 Eltonian niches describe the functional role and biotic interactions of species (Soberón 56 2007). 57 When exotic species are confronted with novel environments to which they need 58 to adjust, they may either keep their niche (niche conservatism) or they may change it 59 (i.e. niche plasticity), and that is true for both the Grinnellian and Eltonian niche. Recent 60 studies have highlighted that many invasive species conserve their Grinnellian niche in 61 their invaded ranges (Wiens et al. 2010; Strubbe et al. 2013), so that Grinnellian niche 62 conservatism has been recognized as the most likely scenario for most bird invaders in 63 Europe (Strubbe et al. 2013). However, Sol et al. (2002) suggested that behavioural 64 flexibility can be important by providing individuals with the ability to expand or 65 change their foraging habits and successfully invade novel environments, representing a 66 change in Eltonian niches. On the other hand, the opposite result (Eltonian niche 67 conservatism and Grinnellian niche shift) has been found in an invasive arthropod, the 68 signal crayfish Pacifastacus leniusculus (Larson et al. 2010), so more studies are called 69 for. 70 Studies on plants have pointed out the importance of differences in the temporal 71 segregation of the niches of species to understand some successful invasions 3 72 (Wolkovich and Cleland 2010), for example because separation in time reduces 73 (competitive) interaction. For other organisms, such as birds, the timing of reproduction 74 of exotic species in their novel environments has been a topic of some historic interest 75 (Baker and Ranson 1938). To maintain viable populations, exotic birds must rapidly 76 adjust to novel environmental conditions (e.g. climate, photoperiod, resources and/or 77 competitors; Blackburn et al. 2009) in the areas of introduction. When introduced, some 78 individuals/species tend to maintain their former reproductive timing (conservatism) 79 whereas others completely change their breeding time (plasticity) (Baker and Ranson 80 1938). As examples of change, House sparrows, Passer domesticus, reproduced 81 continuously during establishment in North America and New Zealand whereas native 82 European sparrows breed seasonally (Hengeveld 1994). At the population level, 83 Rufous-collared Sparrows, Zonotrichia capensis, changed from continuous breeding in 84 their native populations in Colombia to seasonal breeding (up to autumn) in an 85 introduced population in the USA (Miller 1965); and several passerines introduced in 86 New Zealand have increased the length of their breeding season relative to the United 87 Kingdom (Evans et al. 2005). However, the role of phenology when studying Eltonian 88 niche overlap (including niche conservatism and niche expansion) mediated via 89 resource competition has been poorly explored in animal invasion biology. 90 Here we compare the reproductive timing of an entire community of established 91 exotic birds of tropical origin with that of the native, temperate bird community using 92 the same habitats, and explore the importance of this temporal niche axis for 93 establishment success. The timing of reproduction is one of the major life history traits 94 involved in the adaptation of birds to their environments (Lack 1968; Murton and 95 Westwood 1977). Birds show dramatic seasonal reorganizations in physiology (e.g. 96 gonadal development), behaviour (e.g. song, courtship) and morphology (e.g. plumage) 4 97 linked to reproduction (Murton and Westwood 1977). Photoperiodic signal is the main 98 driver regulating the timing of reproduction in birds (Dawson et al. 2001; Hahn and 99 MacDougall-Shackleton 2008), although circannual programming is also known to be 100 important (Helm et al. 2009; Visser et al. 2010). As individuals should reproduce at the 101 right time to maximize their fitness (Martin 1987; Daan et al. 1988; Thomas et al. 2001; 102 Sanz et al. 2003), typically when food availability is maximal, additional cues such as 103 temperature, rainfall, or social factors can fine-tune the timing of reproduction to local 104 conditions (Hahn et al. 1997; Ball and Ketterson 2008; Hau et al. 2008). Thus, 105 differences in timing of reproduction are common between and within species (Hahn et 106 al. 1997), showing typical geographical patterns. For example, in temperate zones, 107 seasonal changes in the environment are highly predictable and most temperate birds 108 breed in spring and early summer, coinciding with the peak of food availability (Cramp 109 and Simmons 1977). In many of those temperate habitats, early breeding is theoretically 110 advantageous because of the higher renesting possibilities and also because fledgling 111 survival and recruitment generally decline with the progression of the breeding season 112 (Lack 1968; Daan et al. 1988; Price et al. 1998; but see Penteriani et al. 2014). On the 113 contrary, postponing reproduction should be disadvantageous if this entails competition 114 for food with migrant or wintering individuals or if ecosystem production (i.e. food 115 resources) decreases with the advancing of the season, potentially leading to partial or 116 total reproductive failure. In contrast, related to the less seasonal climate, tropical birds 117 show a wider range of breeding strategies, from seasonal to opportunistic and 118 continuous breeding (Hau et al. 2008). In general, timing of reproduction among 119 tropical birds is expected to be wider and more asynchronous at the population level 120 than among temperate birds (Hau et al. 2008). 5 121 Establishment success depends on the invader´s ability to fit the ecological 122 characteristics of the recipient community. Competition can be an important factor 123 precluding biological invasions (Sol et al. 2012a; Hernández-Brito et al. 2014) such that 124 exotic species which are functionally different from those already present in the 125 community are more likely to become invaders than species having to face competition 126 with natives (formally called the empty niche, the invasion window or the opportunity 127 window hypotheses; Catford et al. 2009). With respect to timing, invaders may then 128 benefit from a potential Eltonian niche opportunity when having a different timing of 129 reproduction compared to native species if this results in a reduction in competition (i.e. 130 ecological release; Levin 2003). However, establishing species may also be selected to 131 be ecologically similar to the native ones, since this is what the environment dictates. 132 With respect to timing, this then predicts that exotic species should have a reproductive 133 timing that is similar to that of the native species (e.g. adjusting the timing of 134 reproduction to the periods of maximum food availability).