Assessing short- and long-term variations in diversity, timing, and body condition of migratory frugivorous birds

1 Assessing shortand long-term variations in diversity, timing, and body condition of migratory frugivorous birds María Campo-Celada1, Irene Mendoza1*, Ana Benítez-López1, Carlos GutiérrezExpósito2, Julio Rabadán-González3, Pedro Jordano1 1Department of Integrative Ecology, Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas, Avda. Américo Vespucio, 26, 41092, Sevilla, Spain. 2Department of Conservation Biology. Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas, Avda. Américo Vespucio, 26, 41092, Sevilla, Spain. 3Observation.org Spain. C/ Gordal 8, 41940 Tomares, Seville, Spain. *Correspondence author. Email: [email protected]s Keywords: avian community, avian diet, frugivory, Mediterranean, migration, phenology, seasonality, seed dispersal .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 2 Abstract 22 Under current global change context, climate change is driving substantial 23 phenological mismatches between plant species and the organisms that rely on them. 24 Given that frugivorous birds are fundamental for forest regeneration, and most of them 25 are migrant species, identifying the effect of global change over them must be a priority. 26 In this study we have analysed changes in the composition, morphometry, and physical 27 condition in an avian community at long- (40 years) and short time (seasonal) spans. 28 Our findings indicate a profound transformation at practically every level of analysis. In 29 40 years, the avian community shows a 66% and 13% decrease of the wintering and 30 seed-disperser species, respectively. Seasonal abundance peaks were advanced in 13 out 31 of 15 species. In addition, we have found a significant 1.5% increase in the 32 morphometric measurements of certain species, supporting findings in previous studies, 33 and also a remarkable general decrease of body condition. Our results point towards 34 land use changes and climate change as the main causes. If this influence continues to 35 rise, biodiversity will likely be irreversibly altered, damaging crucial ecosystem 36 functions such as animal-mediated seed dispersal and forest regeneration in particular. 37 38 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 3 Introduction 39 Global change drivers are profoundly altering Earth’s biodiversity, ecological 40 systems, and the timing of organisms’ life cycles, i.e., their phenology (Bellard et al., 41 2014; Hansen et al., 2001; Pachauri et al., 2014). In particular, avian communities are 42 undergoing major changes in their abundance (Inger et al., 2014; Studds et al., 2017), 43 composition, and migratory timing due to land use modifications and alterations of 44 climatic conditions (Fischer et al., 2018; Socolar et al., 2016). These changes result in a 45 widespread decline of several bird species around the globe that, although apparent 46 since the 1980s, has experienced its greatest fall in the last pair of decades (Howard et 47 al., 2020; Wilcove & Terborgh, 1984). 48 Among bird species, those that undertake migratory movements are under a 49 strong selection because of their site fidelity and fine tuning with available resources. 50 As a result, they are highly susceptible to ecosystem perturbations, compromising 51 returning flights to breeding grounds or resource tracking, for instance (Cuadrado, 1992; 52 Howard et al., 2020; Winger et al., 2019). Thereby, current global change has increased 53 already high migratory pressures over those species, which translates into changes in 54 community composition both in abundance and species turnover over both shortand 55 long-term scales (Howard et al., 2020; Socolar et al., 2016; Wilcove & Terborgh, 1984). 56 Its impact has also proven noticeable in bird species’ morphological trends (e.g., Weeks 57 et al., 2019). 58 Probably the most overlooked and yet undefined global change-driven effect is 59 related to species phenological mismatches, which occur when there is a temporal 60 uncoupling of interacting organisms. An interesting example is migratory fruit61 dependent birds and their food plants (Snow & Snow, 1988). Frugivorous birds rely on 62 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 4 fleshy fruits for acquiring the nutritional and energetic resources needed for breeding 63 and migrating (Jordano, 2014). This means the timing of bird arrival or fattening needs 64 to match the timing of fruit crops ripening so that birds can acquire the necessary 65 nutrients for breeding or building up the fat accumulation for migration; meanwhile the 66 fruits are consumed and their seeds effectively dispersed. Yet, climate change is 67 profoundly altering species phenology, resulting in temporal uncouplings. Birds had 68 advanced, for instance, their reproductive cycles and arrival dates when food resources 69 are not at their maximum peak availability, with negative consequences for offspring 70 survival, bird condition and the potential recruitment of biotically-dispersed plant 71 species (see e.g., Nowak et al., 2019; Saino et al., 2011; Visser et al., 1998). 72 Such temporal uncouplings generate a substantial decrease in the probability of 73 interspecific encounters between interacting partners and may eventually result in the 74 loss of the ecological pairwise interaction. When interactions disappear, the associated 75 ecological functions and services are lost (Valiente-Banuet & Verdú, 2013), with 76 pervasive consequences for ecosystem dynamics (Aamidor et al., 2011; Blendinger et 77 al., 2015; Carnicer et al., 2009; Cooper et al., 2015; Jordano, 1988). For instance, 78 increased warming has substantially advanced the first flowering date of many plant 79 species from the Northern Hemisphere (Menzel et al., 2006), triggering phenological 80 uncouplings with the emergence of pollinator species. Moreover, global changes have 81 impacted on birds’ body condition and morphological traits, as well as phenology and 82 reproductive success (Bailey et al., 2020; Cooper et al., 2015). However, the empirical 83 data on these temporal mismatches and timing shifts in natural processes are very 84 limited. 85 Migratory birds have been found to show reductions in size over the last 86 decades. For instance, using a four-decade series of specimens from North America, 87 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 5 Weeks et al. (2019) showed a consistent decrease in body size across different taxa, 88 coupled with a general increase in birds’ wing length. Body size reductions are likely to 89 lead to a change in shape that compensates for increasing selective pressures in 90 migratory bird species (Weeks et al., 2019; Winkler & Leisler, 1992). The most 91 common shape transformations are elongation of upper limbs, but wing chord and tarsus 92 length decreases have also been reported in other studies, with meaningful differences 93 found between shortand long-distance migratory species (Van Buskirk et al., 2010; 94 Weeks et al., 2019; Winkler & Leisler, 1992). General trends of body change in bird 95 species are difficult to discern, being ultimately related to not only biological factors but 96 also measuring protocols (Labocha & Hayes, 2012). In the short-term, body and fat 97 mass fluctuations that are consistent with long-term reductions have been reported, but 98 they seem to be mainly related to food availability and seasonal weather (Hampe, 2008; 99 Smith, 2016; Tellería et al., 2013; Weeks et al., 2019), which also has a remarkable 100 impact on migration success (Rojas et al., 2019). Both longand short-term trends in 101 body and fat mass were found consistent with a response to a warmer climate (Gardner 102 et al., 2014; Van Buskirk et al., 2010; Weeks et al., 2019). By finding overall trends 103 across species types, locations, and environmental heterogeneity we could identify 104 generalities that will help forecasting future impacts of global change. We aim to 105 provide empirical evidence to test these predictions by analysing changes (long-term) in 106 wing, tail, tarsus and bill lengths, and changes in fat accumulation (short-term) between 107 decades. 108 Although fat accumulation is a frequently used proxy for physical condition, 109 morphometric indices of body condition have been found to be more reliable, yet 110 usually well-correlated with fat content (Labocha & Hayes, 2012), or lean dry mass in 111 birds (Schulte-Hostedde et al., 2005). There is no universal-best body condition index, 112 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 6 but weight/tarsus residuals based on ordinary least squares regression are independent 113 of the size measurements (predictors; Labocha & Hayes, 2012), and seem to be the best 114 body condition index in our case. Migratory birds’ body condition is determinant on 115 timing, route choice and migration fitness (Bairlein & Gwinner, 1994; Duijns et al., 116 2017); and body condition relies, for strong frugivorous species, mainly on the 117 availability of appropriate fruit resources (in quantity and quality) to support the 118 energetic demands of migration (Bairlein & Gwinner, 1994; Brown & Sherry, 2006; 119 Parrish, 1997; Stoate & Moreby, 1995). We wanted to check whether body condition120 fruit variability matching is different now compared to the 1980s, both at seasonal and 121 interannual scales, given that possible disturbances on fruit production at the stopover 122 area may lead to major ecological consequences. 123 Although there is ample evidence that birds’ phenology changes as a 124 consequence of direct and indirect effects of climate change, such as food scarcity 125 (especially critical in migratory birds), and mismatches between food peak and breeding 126 periods (Haest et al., 2020; Koleček et al., 2020; van Schaik et al., 1993), few studies 127 have the opportunity to test seasonal variations using a standardized methodology over 128 the long-term. In this study, we focused on frugivorous birds, the long-term changes in 129 community composition and diversity, and their changes over time in morphology and 130 body condition related to fruit availability. We used data on bird abundances and 131 morphometry at two different time scales: short- (with biweekly censuses) and long132 term (with historical - 1981-1983 - and current data - 2019-2020; see below). We 133 assessed abundance-based community changes and species turnover in different 134 migratory, trophic, and functional groups. We intended to gain insight in how bird 135 abundances, diversity, phenological timing, body condition and morphology may have 136 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 7 been altered in a 38-year period in a Mediterranean sclerophyllous shrubland 137 community. In particular, we aimed to answer the following four specific questions: 138 (1) How has the avian community changed between the 1980s (1980-1983) and 139 2019-2020 period? What is the extent of turnover for species with different migratory 140 behaviour, trophic level, and ecological function? 141 (2) Is there a seasonal variation in bird abundances? 142 (3) What are the temporal changes in birds’ body size over longand short-term 143 scales? Are there differences among resident and migrant frugivorous species? 144 (4) How does birds’ physical condition change at seasonal and interannual 145 scales? 146 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 8 Materials and methods 147 Study site 148 Location 149 The study area was located in Hato Ratón, a locality immersed in Doñana’s 150 Natural Area, close to Villamanrique de la Condesa, Sevilla province, southern Spain 151 (37° 10' 26.4" N, 6° 20' 17.4" W, 11 m a.s.l.). Doñana’s Natural Area is an Andalusian 152 protected area of almost 122,500 ha that has been widely studied due to its singular 153 biodiversity. As a natural open space situated at one of Europe’s most southerly points, 154 it is a common breeding and nesting spot for bird species that migrate between Europe 155 and North Africa. Its large abundance of fleshy-fruited shrubs attracts a particularly 156 high number of frugivorous bird species of different migratory behaviours, which 157 makes it a suitable location for our project. The vegetation of the site is characterized 158 by tall, diverse, sclerophyllous shrubland on sandy soils dominated by Pistacia lentiscus 159 (Anacardiaceae) and Olea europaea var. sylvestris (Oleaceae) intermingled with Pinus 160 pinea trees (Table S1). 161 Climate 162 The climate of the study area is typically Mediterranean, with hot and drought 163 periods in the summer that contrast with concentrated rainy months in spring and early 164 autumn. Extreme events are also common in terms of drought or heavy rainfall. 165 Average annual mean temperature and accumulated rainfall in the 1980s were 16.7 ºC 166 and 547 mm, respectively, while in the 2010-2019 decade these values were 17.6 ºC and 167 497 mm (Table S2; 1980-2020 series, data from a weather station placed at Doñana 168 Biological Reserve, 20 km from the study area). While mean and minimum 169 temperatures show a slow increasing trend, accumulated rainfall is considerably 170 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 9 variable among years and decades. It is remarkable that the pair of years of the first 171 study period (1981-1983) were exceptionally dry within the decade; accumulated 172 rainfall per month barely surpassed the 300 mm. Also, monthly minimum temperatures 173 were colder in 1981-1983 than the whole 80s-90s period. 174 Data collection 175 Data were collected periodically between January 1981 to October 1983, and 176 again between July 2019 to March 2020, which we will refer to these two time periods 177 as the 1980s and 2019-2020 respectively. Data for the 1980s period were previously 178 available, concerning fruiting phenology and fleshy-fruit production, bird community 179 composition, bird morphometry and body condition, diet composition, etc. (Jordano, 180 1984, 1985, 1987, 1988). Sampling frequency differed between decades, being weekly 181 during the 1980s and biweekly in 2019-2020 (Figure S1). 182 Bird sampling 183 Between 6 and 10 nets were operated weekly during 1981-1983 and 12-20 184 biweekly in 2019-2020. Mist nets were opened from dawn to dusk (1981-1983) or 185 midday (2019-2020) and checked at hourly intervals. Trapped birds were collected 186 individually in fabric bags and then identified and measured by expert ringers following 187 the standard procedures of the EURING criteria. Individual birds were ringed, and the 188 following variables were recorded: species, age, sex, type of moult, existence of brood 189 patch, fat and muscle and also measured body mass (±0. 5 g) and wing, F8 feather, tail, 190 tarsus, and bill (culmen) lengths (± 0.1 mm; ± 0.5 mm for wing, F8 feather, and tail). 191 We checked for data repeatability to assure that measurements between different ringers 192 were significantly consistent. We obtained a significantly high correlation between 193 measures performed by different ringers (r = 0.92-0.99 for all measurement variables, 194 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 16 All analyses were performed in R Statistical Software v. 3.6.2 (R Core Team, 338 2019). Repeatability coefficients were calculated using the “rptR” package (Stoffel et 339 al., 2017). Species turnover was calculated using the “turnover” function included in the 340 “codyn” package (Hallet et al., 2020). The selection of the ANOVAs models was based 341 on the “aictab” function included in “AICcmodavg” package (Mazerolle, 2020). 342 343 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 17 Results: 344 Community composition, bird abundance and species turnover across periods 345 We found a species beta-turnover of the 20 most abundant species of 0.52, with 346 the same proportion (0.26) of species losses and gains between 1981-1983 and 2019347 2020 (Table 1). This means that half of species per decade had reduced their relative 348 abundance and disappeared from the 1981-1983 “top 20” list, being replaced in 2019349 2020 by new birds that were not present or were scarce in 1980s records (Figure S4). 350 We found that the number and abundance of resident bird species have increased, with a 351 0.55 beta-turnover between study periods. The proportion of gained and lost species 352 was 0.35 and 0.20, respectively, and the relative abundance of resident species increased 353 from 60% to 80%, approximately (Figure 1.A). In turn, we found that the relative 354 abundance of the four main wintering bird species has fallen almost two thirds (66%) 355 between 1981-1983 and the current period (Table 1 and Figure 1.A). The abundance 356 proportions of frugivores and non-frugivores showed practically no change between 357 study periods (Figure 1.B), but both groups had gone through a considerable species 358 turnover, especially among the non-frugivores (with a turnover value of 0.60, versus 359 0.47 in frugivores). On one hand, the fruit-eating species as a group maintained its 360 relative abundance, whilst the proportion of new species was lower than the proportion 361 of lost species (0.18 against 0.29). On the other hand, non-frugivore species (granivore, 362 insectivore, granivore-insectivore, and herbivore species) also maintained their 363 abundance but gained the double of species they lost from 1981-1983 to present (0.40 364 against 0.20). 365 Regarding species' functional groups, birds acting as legitimate seed dispersers 366 have also experienced a decrease in their relative abundance from almost 75% to 62% 367 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 18 (see Figure 1.C), with a beta-turnover value of 0.53, and a negative balance of gained 368 versus lost species (0.22 and 0.33). In contrast, non-seed dispersers have become more 369 abundant, with a high turnover value of 0.60 that reflects twice as much gained as lost 370 species (0.40 and 0.20). 371 Seasonal variation in bird abundances 372 From the 23 species analysed, 8 of them were solely recorded in one study 373 period (7 new species in 2019-2020, and one disappeared; Figure 2). Within the 374 remaining 15 species, we identify peak advancement shifts in 13 of them (10 resident 375 and 3 wintering species), one single delay in wintering P. collybita, and no apparent 376 change in F. coelebs. A binomial test using the 13 spp. over 15 indicates a consistent, 377 highly significant (p-value: 0.0074), trend across species towards earlier phenologies in 378 the area. 379 Considering the 23 species trophic types (Table S3), 14 of them have, at least 380 partially, a frugivorous diet and 9 of them never or hardly ever feed on plant fruits. We 381 identified advancements of the maximum abundance date in 11 frugivorous species: C. 382 melanocephala, C. undata, C. chloris, E. rubecula, L.meridionalis, P. major, S. 383 atricapilla, S. rubicola, S. unicolor, T. merula and T. philomelos; and in C. carduelis 384 among the non-frugivorous species. On the other hand, the only phase delay belongs to 385 the largely insectivorous P. collybita (Common Chiffchaff), which also experienced a 386 considerable increase in abundance in January-February. The other species whose 387 increase deserves to be mentioned are C. melanocephala, C. chloris, P. major and S. 388 unicolor, almost doubling their abundances in peak months (Figure 2). 389 With respect to functional types, 13 out of the 14 mentioned frugivorous species 390 are also legitimate seed dispersers, except C. chloris, which is a seed predator (Table 391 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 19 S3). Therefore, their phenological patterns are practically identical to those previously 392 mentioned: 13 seed disperser bird species from which 10 show a marked advance in the 393 peak abundance date (Figure 2). 394 Moreover, when grouping all recorded species’ phenological data into migratory 395 categories (resident, wintering, summering and transient) we observed an overall peak 396 advancement in both resident and wintering species (Figure S3): as we can infer from 397 species’ specific phenological analyses, the general peak advancement in both resident 398 and wintering species is also noticeable in the collapsed resident and wintering groups, 399 respectively. The summering and transient species’ groups were not large enough to 400 elucidate consistent changes. Mann-Whitney tests revealed that monthly abundances 401 significantly differed between study periods in resident (p<< 0.01), wintering (p < 0.05), 402 frugivore (p << 0.01) and non-frugivore (p << 0.01) species groups. 403 Temporal changes in birds’ body size at longand short-term scales 404 All models including morphometric variables showed lower AIC values when 405 including study period, migrant category, species, and interactions as parameters, 406 although sex was only included for wing and tail length (Table 2). The ANOVA’s tests 407 results showed a significant difference in the four body components that can be 408 explained by study period, migrant categories, species and, except in tarsus length, also 409 by sex variables. We also found significant interactions among study periods and 410 migrant categories in tarsus length, and among study periods and recorded species in 411 bill length. 412 We found a significant difference among resident and wintering species in wing, 413 tail, and bill lengths, but not in tarsus length. Regarding species-specific changes in 414 morphometry, we only found significant differences in three species (Figure 3). Tail 415 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 20 length has significantly increased over time for two wintering species: S. atricapilla 416 (+1.46 %) and E. rubecula (+1.9 %), whereas wing length has increased significantly 417 for S. atricapilla only (+1.18 %). Finally, tarsus length has significantly increased in 418 resident C. chloris (+1.4 %). Unequal sample size among the two study time periods 419 might be hindering significance for the tail length increase in n T. merula or bill 420 decrease found in P. collybita case. 421 The GLM’s results show that birds’ body fat accumulation varied significantly 422 between study periods and within migratory seasons (Table 4.A). Birds with a low 423 accumulation of fat in their bodies represented more than 65% of captured individuals 424 in both decades, whilst birds with medium or high fat accumulation accounted for less 425 than one-third of captures in each period respectively (Figure 4). We found two 426 different patterns among year groups: in 1981-1983, medium-high fat accumulation 427 peaked at the migratory pass, while in 2019-2020 it occurred at the autumn step. Low 428 fat accumulation individuals seem to be more, or at least equally, common among 429 migratory seasons, while birds with medium-high fat have been less detected in 2019430 2020, especially during the migratory pass season. 431 Change in body condition at seasonal and interannual scale 432 We found significant differences in body condition among study periods and 433 migratory categories, as well as statistically significant interactions between both factors 434 (Table 4.B). Generally, we recorded more individuals with a good body condition in 435 1981-1983 than in 2019-2020, with a higher median value in Figure 5.A. Over a 436 seasonal scale (Figure 5.B), we also obtained a trend for higher median body condition 437 monthly value in 8 out of 9 study months when comparing 1981-1983 vs. 2019-2020; 438 pointing to a consistent trend towards reduced general body condition along the year in 439 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 21 Hato Raton’s 2019-2020 avian community. At the species level, we identified 7 out of 8 440 species that presented a relative decrease of mean body condition, although the change 441 was more pronounced for T. merula (Figure 5.C). Only Erithacus rubecula showed 442 better body condition in 2019-2020 compared with 1981-1983, meaning that a higher 443 proportion of residuals were above 0 in this particular species. 444 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 22 Discussion 445 In this study, we explored bird community changes over a 40 year-time span 446 between annual cycles of 1981-1983 and 2019-2020, aiming to test whether avian 447 communities showed significant changes over time in diversity, phenology, 448 morphometry, and body condition. Our results indicate that the avian community is 449 effectively altered in all these aspects, with lasting consequences for ecosystem services 450 and biodiversity conservation. 451 Community composition 452 We have observed a remarkable transformation in Hato Raton’s bird community 453 composition and beta-diversity, with more than half of the main species replaced from 454 1981-1983. We found out that migrant species are less common in number and 455 abundance, recording a 66 % decrease in wintering species abundance, though we did 456 not detect species turnover in this group, and barely recording transient species in 2019457 2020. Together with these losses of migrant species, we also recorded fewer frugivorous 458 and legitimate seed-disperser bird species; resident species that are non-frugivorous and 459 non-disperser were more abundant and rich in number, almost doubling gains in the 460 2019-2020 records. As migrant birds are likely to find adverse conditions at several 461 points of their migratory routes (Wilcove & Terborgh, 1984), it is difficult to discern the 462 most significant causes of their population decline. Population shifts of European 463 migrant species have been found to be firmly related to climatic conditions on breeding 464 and wintering grounds (such as our study area) and provenance areas, but are also likely 465 to be strongly related to land-use changes (Bellard et al., 2014; Howard et al., 2020). 466 For instance, a warmer climate in northern areas could provide enough resources and a 467 more suitable environment for breeding or even wintering, reducing the need for long468 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 23 distance flights to find southernmost breeding areas. As species may have started 469 breeding at increasingly higher latitudes, the bird arrival contingent could be reduced in 470 our study area. Moreover, as species differ in their resource tracking capability in 471 shifting scenarios, the more dispersive taxa could be the ones capable of returning to 472 traditional breeding areas (Socolar et al., 2016). Our results are consistent with these 473 interpretations, yet broader-scale data from the Mediterranean Basin would be necessary 474 to test the consistency of these trends in different areas. 475 Vegetation change in our study area could be another possible explanation for 476 our findings. We detected a considerable increase of forest cover, taller vegetation 477 physiognomies, and a reduction of the cover of fleshy-fruited species, transforming our 478 study area from a shrub-dominated area in the 1980s to an area with larger abundance of 479 pines with poorer understory at present. Transformation of Hato Ratón’s vegetation 480 could directly affect migratory-species habitat selection, as they are commonly found to 481 prefer wide open spaces in edge-type areas in which shrublands with fleshy-fruited 482 species dominate (Zamora et al. 2010). Therefore, spatial distribution of vegetation, 483 changes in plant community structure, and fleshy-fruited plant abundance could explain 484 our diminished detection of migrant birds due to habitat selection, despite breeding 485 ground site fidelity. 486 Also, we cannot discount the profound transformation that Doñana’s Natural 487 Area has experienced over the last decades. From being a natural space of remarkable 488 plant and animal biodiversity, it has been seriously degraded by agricultural human 489 action. One of the most attractive areas for birds in Doñana, the marshlands, have 490 experienced a 82 % reduction from the beginning of the 20th century to the 2000s 491 decade, mainly as a consequence of human-induced changes, such as desiccation for 492 agricultural land and modification of stream channels (Haberl et al., 2009), both 493 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 24 exacerbated by changes in the climatic conditions towards higher temperatures and less 494 predictable precipitation. A final explanation for the observed decrease of migrant 495 species could be the simultaneous enhancement of the resident species local population. 496 As a consequence of area transformation, available resources may not be sufficient to 497 support an avian community as large as in the 1980s. Resident species could prove to be 498 superior competitors, choosing the best feeding areas before migrant species arrive. For 499 instance, de la Hera et al., (2018) found that Erithacus rubecula’s resident populations 500 in S Spain tend to occupy woodlands, unlike their migrant conspecifics, which occupy 501 shrublands. This is likely to play a role in the development of local adaptations for the 502 different habitats in the breeding grounds. Similarly, resident individuals of Sylvia 503 atricapilla in S Spain are larger in body size and tend to be more abundant in forests 504 (Pérez-Tris & Tellería, 2002), suggesting an advantage over their migrant conspecifics. 505 Overall, vegetation shifts towards greater arboreal cover appear to have favoured a 506 reduced representation of migrants vs. the resident assemblage. 507 The reduction of legitimate seed-disperser species associated with migrant bird 508 declines could have a major impact on ecosystem function and services (Inger et al., 509 2014). As interactions are often lost well before species completely disappear (Valiente510 Banuet et al., 2015), a reduction of seed dispersers may immediately impact ecosystem 511 functioning, with a potential reduction of plant seed dispersal success and, therefore, 512 direct consequences for the recruitment of fleshy-fruited species and plant community 513 composition. Due to the progressive disappearance of these crucial species, plants 514 whose reproduction relies on them may become less abundant in favour of other plants 515 with abiotic seed dispersal, resulting in a change in plant composition. We have 516 possibly detected this effect in the huge expansion of Pinus pinea conifer in our study 517 plots, although this hypothesis warrants further investigation. If this trend is maintained 518 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 25 in the coming years, our study area would become increasingly homogeneous, leading 519 to a complete reorganization of the avian community and the fleshy-fruited plants that 520 depend upon it, ultimately leading to an undesirable ecological collapse. 521 Bird timing 522 At a seasonal scale, we found consistent shifts among resident and wintering523 species’ seasonal abundance distributions, identifying 13 trends for advancement shifts 524 and a single species, out of a total 15, showing a delay when comparing 1981-1983 vs. 525 in 2019-2020. The proportion of advancement trends versus delays is practically the 526 same within migratory (resident and wintering), trophic (frugivore and non-frugivore) 527 and functional (seed disperser and non-disperser) categories, revealing a consistent and 528 significant shift towards earlier abundance peaks among species. 529 Due to the lack of continuity between our sampled time points, our results 530 cannot be explained in terms of long-term trends along a temporal series on an annual 531 basis. However, these changes in seasonal abundances are highly relevant and in 532 correspondence with reported temporal advances of migrant species arrival to their 533 wintering grounds as a response to warmer temperatures (Butler, 2003; Haest et al., 534 2020; Koleček et al., 2020). Migratory behaviour has been widely attributed as a 535 resource tracking mechanism of birds with enough phenotypic plasticity to adapt their 536 timing to shifting food-resource peaks (Haest et al., 2020; van Schaik et al., 1993): 537 whilst plant-feeding species seem to be able to match earlier plant production, birds 538 with an insectivore diet seem to be less headed towards phase advancements (Butler, 539 2003). This could be the explanation for the lack of seasonal change in abundance found 540 for P. collybita. Nevertheless, a complex set of factors could ultimately drive bird 541 phenological advancement: climatic conditions in departure areas could delay departure 542 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 32 Brown, D. R., & Sherry, T. W. (2006). Food supply controls the body condition of a 672 migrant bird wintering in the tropics. Oecologia, 149(1), 22-32. 673 https://doi.org/10.1007/s00442-006-0418-z 674 Butler, C. J. (2003). The disproportionate effect of global warming on the arrival dates 675 of short-distance migratory birds in North America. Ibis, 145(3), 484-495. 676 https://doi.org/10.1046/j.1474-919X.2003.00193.x 677 Carnicer, J., Jordano, P., & Melián, C. J. (2009). The temporal dynamics of resource use 678 by frugivorous birds: A network approach. Ecology, 90(7), 1958-1970. 679 https://doi.org/10.1890/07-1939.1 680 Cooper, N. W., Sherry, T. W., & Marra, P. P. (2015). Experimental reduction of winter 681 food decreases body condition and delays migration in a long-distance migratory 682 bird. Ecology, 96(7), 1933-1942. https://doi.org/10.1890/14-1365.1 683 Cuadrado, M. (1992). Year to year recurrence and site‐fidelity of blackcaps Sylvia 684 atricapilla and robins Erithacus rubecula in a Mediterranean wintering area. 685 Ringing & Migration, 13(1), 36-42. 686 https://doi.org/10.1080/03078698.1992.9674013 687 Duijns, S., Niles, L. J., Dey, A., Aubry, Y., Friis, C., Koch, S., Anderson, A. M., & 688 Smith, P. A. (2017). Body condition explains migratory performance of a long689 distance migrant. Proceedings of the Royal Society B: Biological Sciences, 690 284(1866), 20171374. https://doi.org/10.1098/rspb.2017.1374 691 Fischer, M., Rounsevell, M., Rando, A. T.-M., Mader, A., Church, A., Elbakidze, M., 692 Elias, V., Hahn, T., Harrison, P. A., Hauck, J., Sandstrom, C., Pinto, I. S., 693 Visconti, P., Zimmermann, N. E., & Christie, M. (2018). Summary for 694 policymakers of the regional assessment report on biodiversity and ecosystem 695 services for Europe and Central Asia of the Intergovernmental Science-Policy 696 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 33 Platform on Biodiversity and Ecosystem Services. IPBES Secretariat. 697 https://pure.aber.ac.uk/portal/cy/publications/summary-for-policymakers-of-the698 regional-assessment-report-on-biodiversity-and-ecosystem-services-for-europe699 and-central-asia-of-the-intergovernmental-sciencepolicy-platform-on700 biodiversity-and-ecosystem-services(3c9a1d4f-117b-4e0a-aa4f701 fc825d0a7180).html 702 Gardner, J. L., Amano, T., Backwell, P. R. Y., Ikin, K., Sutherland, W. J., & Peters, A. 703 (2014). Temporal patterns of avian body size reflect linear size responses to 704 broadscale environmental change over the last 50 years. Journal of Avian 705 Biology, 45(6), 529-535. https://doi.org/10.1111/jav.00431 706 Gill, F., Donsker, D. & Rasmussen, P. (Eds). 2020. IOC World Bird List (v10.2). doi : 707 10.14344/IOC.ML.10.2 708 Goodman, R. E., Lebuhn, G., Seavy, N. E., Gardali, T., & Bluso-Demers, J. D. (2012). 709 Avian body size changes and climate change: Warming or increasing 710 variability? Global Change Biology, 18(1), 63-73. 711 https://doi.org/10.1111/j.1365-2486.2011.02538.x 712 Gordo, O. (2007). Why are bird migration dates shifting? A review of weather and 713 climate effects on avian migratory phenology. Climate Research, 35, 37-58. 714 https://doi.org/10.3354/cr00713 715 Haberl, H., Gaube, V., Díaz-Delgado, R., Krauze, K., Neuner, A., Peterseil, J., Plutzar, 716 C., Singh, S. J., & Vadineanu, A. (2009). Towards an integrated model of 717 socioeconomic biodiversity drivers, pressures and impacts. A feasibility study 718 based on three European long-term socio-ecological research platforms. 719 Ecological Economics, 68(6), 1797-1812. 720 https://doi.org/10.1016/j.ecolecon.2008.11.013 721 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 34 Haest, B., Hüppop, O., & Bairlein, F. (2020). Weather at the winter and stopover areas 722 determines spring migration onset, progress, and advancements in Afro723 Palearctic migrant birds. Proceedings of the National Academy of Sciences, 724 201920448. https://doi.org/10.1073/pnas.1920448117 725 Hampe, A. (2008). Fruit tracking, frugivore satiation, and their consequences for seed 726 dispersal. Oecologia, 156(1), 137-145. https://doi.org/10.1007/s00442-008727 0979-0 728 Hansen, A. J., Neilson, R. P., Dale, V. H., Flather, C. H., Iverson, L. R., Currie, D. J., 729 Shafer, S., Cook, R., & Bartlein, P. J. (2001). Global Change in Forests: 730 Responses of Species, Communities, and Biomes. Interactions between climate 731 change and land use are projected to cause large shifts in biodiversity. 732 BioScience, 51(9),765-779. 733 https://doi.org/10.1641/00063568(2001)051[0765:GCIFRO]2.0.CO;2 734 Hera, I. D. L., Fandos, G., Fernández-López, J., Onrubia, A., Pérez-Rodríguez, A., 735 Pérez-Tris, J., & Tellería, J. L. (2018). Habitat segregation by breeding origin in 736 the declining populations of European Robins wintering in southern Iberia. Ibis, 737 160(2), 355-364. https://doi.org/10.1111/ibi.12549 738 Howard, C., Stephens, P. A., Pearce-Higgins, J. W., Gregory, R. D., Butchart, S. H. M., 739 & Willis, S. G. (2020). Disentangling the relative roles of climate and land cover 740 change in driving the long-term population trends of European migratory birds. 741 Diversity and Distributions, In Press. https://doi.org/10.1111/ddi.13144 742 Inger, R., Gregory, R., Duffy, J. P., Stott, I., Vorisek, P., & Gaston, K. J. (2015). 743 Common European birds are declining rapidly while less abundant species’ 744 numbers are rising. Ecology Letters, 18:28–36 https://doi.org/10.1111/ele.12387 745 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 35 Jordano, P. (1984a). Relaciones entre plantas y aves frugivoras en el matorral 746 mediterráneo del área de Doñana. PhD Dissertation, University of Seville. 747 https://dialnet.unirioja.es/servlet/tesis?codigo=23313 748 Jordano, P. (1984b). Seed Weight Variation and Differential Avian Dispersal in 749 Blackberries Rubus ulmifolius. Oikos, 43(2), 149-153. JSTOR. 750 https://doi.org/10.2307/3544762 751 Jordano, P. (1985). El ciclo anual de los Paseriformes frugívoros en el matorral 752 mediterráneo del sur de España: Importancia de su invernada y variaciones 753 interanuales. Ardeola, 32(1): 69-94. https://digital.csic.es/handle/10261/45077 754 Jordano, P. (1987). Frugivory, external morphology and digestive system in 755 mediterranean sylviid warblers Sylvia spp. Ibis, 129(S1), 175-189. 756 https://doi.org/10.1111/j.1474-919X.1987.tb03199.x 757 Jordano, P. (1988). Diet, fruit choice and variation in body condition of frugivorous 758 warblers in mediterranean scrubland. Ardea, 76, 193-209. 759 Jordano, P. (2014). Fruits and frugivory. In Gallagher, R. S. (2014). Seeds, 3rd Edition: 760 The Ecology of Regeneration in Plant Communities. CABI. pp 18-41. 761 Koleček, J., Adamík, P., & Reif, J. (2020). Shifts in migration phenology under climate 762 change: Temperature vs. abundance effects in birds. Climatic Change.159:177763 194. https://doi.org/10.1007/s10584-020-02668-8 764 Labocha, M. K., & Hayes, J. P. (2012). Morphometric indices of body condition in 765 birds: A review. Journal of Ornithology, 153(1), 1-22. 766 https://doi.org/10.1007/s10336-011-0706-1 767 Lank, D. B., Xu, C., Harrington, B. A., Morrison, R. I. G., Gratto‐Trevor, C. L., 768 Hicklin, P. W., Sandercock, B. K., Smith, P. A., Kwon, E., Rausch, J., Dominix, 769 L. D. P., Hamilton, D. J., Paquet, J., Bliss, S. E., Neima, S. G., Friis, C., 770 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 36 Flemming, S. A., Anderson, A. M., & Ydenberg, R. C. (2017). Long-term 771 continental changes in wing length, but not bill length, of a long-distance 772 migratory shorebird. Ecology and Evolution, 7(9), 3243-3256. 773 https://doi.org/10.1002/ece3.2898 774 Menzel, A., Sparks, T. H., Estrella, N., & Roy, D. B. (2006). Altered geographic and 775 temporal variability in phenology in response to climate change. Global Ecology 776 and Biogeography, 15(5), 498-504. https://doi.org/10.1111/j.1466777 822X.2006.00247.x 778 Miles, D. B., & Ricklefs, R. E. (1984). The Correlation Between Ecology and 779 Morphology in Deciduous Forest Passerine Birds. Ecology, 65(5), 1629-1640. 780 https://doi.org/10.2307/1939141 781 Moller, A. P., Rubolini, D., & Lehikoinen, E. (2008). Populations of migratory bird 782 species that did not show a phenological response to climate change are 783 declining. Proceedings of the National Academy of Sciences, 105(42), 16195784 16200. https://doi.org/10.1073/pnas.0803825105 785 Nowak, L., Kissling, W. D., Bender, I. M. A., Dehling, D. M., Töpfer, T., Böhning786 Gaese, K., & Schleuning, M. (2019). Projecting consequences of global 787 warming for the functional diversity of fleshy-fruited plants and frugivorous 788 birds along a tropical elevational gradient. Diversity and Distributions, 25(9), 789 1362-1374. https://doi.org/10.1111/ddi.12946 790 Nowakowski, J. J. (2000). Long-Term Variability of Wing Length in a Population of the 791 Reed Warbler Acrocephalus scirpaceus. Acta Ornithologica, 35(2), 173-182. 792 https://doi.org/10.3161/068.035.0210 793 Pachauri, R. K., Allen, M. R., Barros, V. R., Broome, J., Cramer, W., Christ, R., 794 Church, J. A., Clarke, L., Dahe, Q., Dasgupta, P., Dubash, N. K., Edenhofer, O., 795 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 37 Elgizouli, I., Field, C. B., Forster, P., Friedlingstein, P., Fuglestvedt, J., Gomez796 Echeverri, L., Hallegatte, S., … van Ypserle, J.-P. (2014). Climate Change 2014: 797 Synthesis Report. Contribution of Working Groups I, II and III to the Fifth 798 Assessment Report of the Intergovernmental Panel on Climate Change. En R. K. 799 Pachauri & L. Meyer (Eds.), EPIC3 Geneva, Switzerland, IPCC, 151 p., pp. 800 151, ISBN: 978-92-9169-143-2 (p. 151). IPCC. 801 https://epic.awi.de/id/eprint/37530/ 802 Parrish, J. D. (1997). Patterns of Frugivory and Energetic Condition in Nearctic 803 Landbirds during Autumn Migration. The Condor, 99(3), 681-697. 804 https://doi.org/10.2307/1370480 805 Pérez-Tris, J., & Tellería, J. L. (2002). Migratory and sedentary blackcaps in sympatric 806 non-breeding grounds: Implications for the evolution of avian migration. 807 Journal of Animal Ecology, 71(2), 211-224. https://doi.org/10.1046/j.1365808 2656.2002.00590.x 809 R Core Team (2019). R: A language and environment for statistical computing. R 810 Foundation for Statistical Computing, Vienna, Austria. URL https://www.R811 project.org/. 812 Rojas, T. N., Vergara-Tabares, D. L., Valdez, D. J., Ponzio, M. F., & Peluc, S. I. (2019). 813 Food supplementation by an invasive fleshy-fruited shrub sustains body 814 condition of a native frugivorous bird during winter. Integrative Zoology, 14(3), 815 259-269. https://doi.org/10.1111/1749-4877.12353 816 Saino, N., Ambrosini, R., Rubolini, D., von Hardenberg, J., Provenzale, A., Hüppop, K., 817 Hüppop, O., Lehikoinen, A., Lehikoinen, E., Rainio, K., Romano, M., & 818 Sokolov, L. (2011). Climate warming, ecological mismatch at arrival and 819 population decline in migratory birds. Proceedings of the Royal Society B: 820 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 38 Biological Sciences, 278(1707), 835-842. 821 https://doi.org/10.1098/rspb.2010.1778 822 Schulte-Hostedde, A. I., Zinner, B., Millar, J. S., & Hickling, G. J. (2005). Restitution 823 of Mass–Size Residuals: Validating Body Condition Indices. Ecology, 86(1), 824 155-163. https://doi.org/10.1890/04-0232 825 Smith, R. J. (2016). Mass Change Values of Landbird Migrants at an Inland Stopover 826 Site Dominated by Nonnative Vegetation. The American Midland Naturalist, 827 175(1), 82-90. https://doi.org/10.1674/amid-175-01-82-90.1 828 Snow, B., & Snow, D. (1988). Birds and Berries. A & C Black Publishers, London. 829 Socolar, J. B., Gilroy, J. J., Kunin, W. E., & Edwards, D. P. (2016). How Should Beta830 Diversity Inform Biodiversity Conservation? Trends in Ecology & Evolution, 831 31(1), 67-80. https://doi.org/10.1016/j.tree.2015.11.005 832 Stoate, C., & Moreby, S. J. (1995). Premigratory diet of trans-Saharan migrant 833 passerines in the western Sahel. Bird Study, 42(2), 101-106. 834 https://doi.org/10.1080/00063659509477156 835 Stoffel, M. A., Nakagawa, S., & Schielzeth, H. (2017). rptR: Repeatability estimation 836 and variance decomposition by generalized linear mixed-effects models. 837 Methods in Ecology and Evolution, 8(11), 1639-1644. 838 https://doi.org/10.1111/2041-210X.12797 839 Studds, C. E., Kendall, B. E., Murray, N. J., Wilson, H. B., Rogers, D. I., Clemens, R. 840 S., Gosbell, K., Hassell, C. J., Jessop, R., Melville, D. S., Milton, D. A., Minton, 841 C. D. T., Possingham, H. P., Riegen, A. C., Straw, P., Woehler, E. J., & Fuller, 842 R. A. (2017). Rapid population decline in migratory shorebirds relying on 843 Yellow Sea tidal mudflats as stopover sites. Nature Communications, 8(1), 844 14895. https://doi.org/10.1038/ncomms14895 845 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 39 Swaddle, J. P., & Lockwood, R. (1998). Morphological Adaptations to Predation Risk 846 in Passerines. Journal of Avian Biology, 29(2), 172-176. JSTOR. 847 https://doi.org/10.2307/3677195 848 Tellería, J. L., Blázquez, M., Hera, I. D. L., & Pérez-Tris, J. (2013). Migratory and 849 resident Blackcaps Sylvia atricapilla wintering in southern Spain show no 850 resource partitioning. Ibis, 155(4), 750-761. https://doi.org/10.1111/ibi.12078 851 Valiente-Banuet, A., Aizen, M. A., Alcántara, J. M., Arroyo, J., Cocucci, A., Galetti, 852 M., García, M. B., García, D., Gómez, J. M., Jordano, P., Medel, R., Navarro, 853 L., Obeso, J. R., Oviedo, R., Ramírez, N., Rey, P. J., Traveset, A., Verdú, M., & 854 Zamora, R. (2015). Beyond species loss: The extinction of ecological 855 interactions in a changing world. Functional Ecology, 29(3), 299-307. 856 https://doi.org/10.1111/1365-2435.12356 857 Valiente-Banuet, A., & Verdú, M. (2013). Plant Facilitation and Phylogenetics. Annual 858 Review of Ecology, Evolution, and Systematics, 44(1), 347-366. 859 https://doi.org/10.1146/annurev-ecolsys-110512-135855 860 Van Buskirk, J., Mulvihill, R. S., & Leberman, R. C. (2010). Declining body sizes in 861 North American birds associated with climate change. Oikos, 119(6), 1047862 1055. https://www.jstor.org/stable/25700339 863 van Schaik, C. P., Terborgh, J. W., & Wright, S. J. (1993). The Phenology of Tropical 864 Forests: Adaptive Significance and Consequences for Primary Consumers. 865 Annual Review of Ecology and Systematics, 24, 353-377. JSTOR. 866 Visser, M. E., Noordwijk, A. J. van, Tinbergen, J. M., & Lessells, C. M. (1998). 867 Warmer springs lead to mistimed reproduction in great tits (Parus major). 868 Proceedings of the Royal Society of London. Series B: Biological Sciences, 869 265(1408), 1867-1870. https://doi.org/10.1098/rspb.1998.0514 870 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 40 Weeks, B. C., Willard, D. E., Zimova, M., Ellis, A. A., Witynski, M. L., Hennen, M., & 871 Winger, B. M. (2019). Shared morphological consequences of global warming 872 in North American migratory birds. Ecology Letters, 23(2), 316-325. 873 https://doi.org/10.1111/ele.13434 874 Wilcove, D., & Terborgh, J. (1984). Patterns of population decline in birds. American 875 Birds, 38:10-13. 876 Winger, B. M., Auteri, G. G., Pegan, T. M., & Weeks, B. C. (2019). A long winter for 877 the Red Queen: Rethinking the evolution of seasonal migration. Biological 878 Reviews, 94(3), 737-752. https://doi.org/10.1111/brv.12476 879 Winkler, H., & Leisler, B. (1992). On the ecomorphology of migrants. Ibis, 134(s1), 21880 28. https://doi.org/10.1111/j.1474-919X.1992.tb04729.x 881 Zamora, R., J. Antonio Hodar, L. Matias, and I. Mendoza. 2010. Positive adjacency 882 effects mediated by seed disperser birds in pine plantations. Ecological 883 Applications 20:1053-1060. 884 885 886 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 41 Tables: 887 Table 1: Species turnover values of different categories (“Groups”) classified according 888 three criteria (“types”). The number of species included in each group is indicated in 889 column “n”. Species’ groups turnover values (“Turnover”) were also split into 890 proportions of species that appeared (“Gained spp.”) and disappeared (“Lost spp.”) in 891 the 2019-2020 period compared to 1981-1983 study years. Observations were also 892 included in the last column. *: Transient and summering species were excluded from 893 migratory category because they were not sampled in 2019-2020. Wintering species 894 were abundant but did not reach 5 spp. per study period needed to calculate turnover. 895 896 897 898 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 48 937 Figure 4: Comparison of seasonal birds’ fat accumulation between study periods 938 (panels “1981-1983” and “2019-2020”), expressed as the percentage of recorded 939 individuals belonging to low fat accumulation (grey colour) or high-medium fat 940 accumulation (orange colour) levels in each migratory season: migratory pass (July941 September), autumn step (October-November) and wintering (December-March). 942 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint 49 943 944 945 Figure 5: Species body condition change between study periods (A), study months (B) 946 and at species’ level (C). Black (A and B) and grey (C) dotted lines separates positive 947 (“good” body condition) and negative residuals (“poor” body condition). A and B body 948 condition values are expressed in logarithmic scale. 949 950 .CC-BY-NC-ND 4.0 International licenseperpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for thisthis version posted October 27, 2020. ; https://doi.org/10.1101/2020.10.27.356709doi: bioRxiv preprint