Multiple components of environmental change drive populations of breeding waders in seminatural grasslands

Abstract Environments are rapidly changing due to climate change, land use, intensive agriculture, and the impact of hunting on predator populations. Here, we analyzed long‐term data recorded during 1928–2014 on the size of breeding populations of waders at two large nature reserves in Denmark, Vejlerne and Tipperne, to determine the effects of components of environmental change on breeding populations of waders. Environmental variables and counts of waders were temporally autocorrelated, and we used generalized least square (GLS) by incorporating the first‐order autoregressive correlation structure in the analyses. We attempted to predict the abundance of waders for short‐term trends for two nature reserves (35 years) and for long‐term trends for one nature reserve (86 years), using precipitation, temperature, nutrients, abundance of foxes Vulpes vulpes, area grazed, and number of cattle. There was evidence of impacts of nutrients, climate (long‐term changes in temperature and precipitation), grazing, mowing, and predation on bird populations. We used standard random effects meta‐analyses weighted by (N–3) to quantify these mean effects. There was no significant difference in effect size among species, while mean effect size differed consistently among environmental factors, and the interaction between effect size for species and environmental factors was also significant. Thus, environmental factors affected the different species differently. Mean effect size was the largest at +0.20 for rain, +0.11 for temperature, −0.09 for fox abundance, and −0.03 for number of cattle, while there was no significant mean effect for fertilizer, area grazed, and year. Effect sizes for two short‐term time series from Tipperne and Vejlerne were positively correlated as were effect sizes for short‐term and long‐term time series at Tipperne. This implies that environmental factors had consistent effects across large temporal and spatial scales.


| INTRODUC TI ON
Breeding populations of waders are declining across western Europe (Thorup, 2006;Roodbergen, van der Wert, & Hötker, 2012;Robinson, Morrison, & Baillie, 2014). The reasons for these declines include intensified agricultural practice, reclamation of coastal habitats, increasing predation pressure, human disturbance, and climate change (Beintema & Müskens, 1987;Wilson, Ausden, & Milsom, 2004;Smart, Gill, Sutherland, & Watkinson, 2006;Holm & Laursen, 2009;Roodbergen et al., 2012;Stephens et al., 2016). Demographic studies show that the declines are mainly caused by poor chick survival rather than adult survival (Roodbergen, Klok, & Schekkerman, 2008;Roodbergen et al., 2012). Low breeding success is caused by losses of nests to predation and flooding (Hötker & Segebade, 2000; Van de Pol et al., 2010;Bellebaum & Bock, 2009;Thorup & Koffijberg, 2016). Studies of wader populations during recent years have focused on farmland revealing complex interactions between agricultural practice and climate, affecting the survival of young (Kleijn et al., 2010;Schroeder et al., 2012). Young waders have to find their own food, and due to high energy requirements and poor abilities to save energy, they operate within narrow energetic margins, for example, a balance between quantity and quality of food (Schekkerman & Visser, 2001;Maier, 2013). To this array of parameters influencing wader populations, we included change in nutrient load in the environment as a proxy for primary productivity and amount of benthos and thus indirectly carrying capacity for breeding birds (Philippart et al., 2007;Møller, Flensted-Jensen, Laursen, & Mardal, 2015). Thus, nutrient load can be an important parameter, although a straightforward relationship between nutrients and amount of invertebrate food for young cannot be expected (Schekkerman & Beintema, 2007). Outside the breeding season during migration and at wintering sites, several wader species stage and forage in marine estuaries and along coasts that are influenced by nutrients (Vitousek, Mooney, Lubchenko, & Melillo, 1997;Windolf, Blicher-Mathiesen, Carstensen, & Krovang, 2012). Different components of environmental change such as climate change, land use, and fisheries are currently being described as determinants of poor reproductive performance, reduced survivorship, and declining population trends for waders and other bird populations (Frederiksen, Wanless, Harries, Rothery, & Wilson, 2004;Schroeder et al., 2012;Maier, 2013). However, few studies have demonstrated for climate change that demographic variables determine population size (Dunn & Møller, 2014;Robinson et al., 2014;Stephens et al., 2016). Attempts to make integrated analyses of the relative contributions of multiple factors accounting for such trends are scarce. A number of studies have recently investigated the effects of climate change and land use on population size (Møller, Flensted-Jensen, & Mardal, 2007;Pimm, 2009;Eglington & Pearce-Higgins, 2012;Mantyka-Pringle, Martin, & Rhodes, 2012;Jørgensen et al., 2015;Martin, van Dyck, Dendoncker, & Titeux, 2013;. This leaves a number of additional factors in need of study, including population changes and effects of industrialized agriculture with high levels of fertilizer use. Since such analyses quickly include many predictors, they are resource demanding and only feasible when based on long-term studies. Unfortunately, most time series in ecological research are short and only rarely exceed 50 years, thereby often preventing inclusion of all or even most crucial predictors and certainly not inclusion of interactions among variables. The aims of this study were (a) to quantify the effect size for the impact of environmental conditions on the population size of seven wader species; (b) to analyze the effects of climate, nutrients, land use, and predator abundance on size of local breeding populations in a 86-year time series of wader bird communities at Tipperne and two short-term time series of 35 years at Tipperne and Vejlerne; (c) to test for consistency in effect size between one short-term and one long-term time series at Tipperne and for one short-term time series of effect sizes at Tipperne and one short-term time series at Vejlerne. We did so by analyzing the breeding abundance of seven wader species during 1928-2014 at the nature reserve Tipperne, Denmark, and during 1978-2014 at the nature reserve Vejlerne, Denmark.

| Sites, wader species, and study periods
We studied breeding waders at two seminatural grassland sites (Tipperne and Vejlerne) in western Denmark extensively farmed, for example, grazed by cattle at low density, late mowing, and without direct use of fertilizer (see site description in Supporting information Appendix S1). We focused on the wader bird community composed of seven species: Oystercatcher Haematopus ostralegus, lapwing

| Census methods
Census methods are described by Møller (1983), Thorup (1998), and Kjeldsen (2008). They have been adjusted during the study period due to change in vegetation height. At Tipperne during 1928-1957, nests were searched intensively. During 1958During -1964, nest searches were supplemented by mapping birds giving alarm calls to identify territories. In 1965-1985, breeding birds giving alarm calls were mapped together with nests. From 1986, breeding waders were mapped from a distance with a telescope (60× magnification) supplemented with mapping events of warning birds. These methods were grouped in three categories and entered in the statistical analyses as a factor with the following levels: nest search, nest search and territory mapping, and territory mapping and telescope use. A detailed description of the census methods is given in Supporting information Appendix S1.

| Climate
Climate estimated as long-term change in precipitation and temperature together with groundwater level is known to affect breeding wader populations (Thorup, 1998;Bellebaum & Bock, 2009;Schroeder et al., 2012;Maier, 2013). We used mean of daily maximum air temperature (°C) in April and sum of monthly precipitation for March, April, and May (mm, data from Danish Meteorological Institute). We used data on climate measured at a local coastal weather station at Vestervig. Groundwater at Tipperne and water level at the outlet sluice at Vejlerne were measured, but not included in the environmental analysis due to significant correlations (p < 0.05) with precipitation in most spring months.

| Nutrients
Data on fertilizer from farmland in Denmark were estimated for 1928-2014 as the annual amount of outlet of total-N (tons) to coastal waters (Conley et al., 2007) and updates by Hansen (2011) and Thodsen et al. (2016). Each update was calibrated to the former level. This data set was used for the long-term statistical analyses for Tipperne. From 1989, data on nitrogen (μg/L) concentration were collected in Ringkøbing Fjord (surrounding Tipperne) and for nitrogen in Limfjorden (adjacent to Vejlerne) as a part of the national monitoring program NOVANA (data from Environment Centre Ringkøbing; both sites; Hansen, 2015). These data sets were used for the short-term statistical analyses at Tipperne and Vejlerne.
We analyzed the effects of foxes on nest predation (Thorup, 1998;Kjeldsen, 2008). Information about fox abundance was taken from the official Danish bag statistics, which goes back to 1941.
From this year up to 1972, we used the national bag size of foxes as a proxy for fox abundance (annual number of foxes shot in Denmark).
From 1973 to 2014, information exists about fox bag at the country level (annual number of foxes shot per county surrounding Tipperne and Vejlerne), and we used this local information to account for differences between regions. Environmental data for Tipperne and Vejlerne are shown in Supporting information Tables S1 and S2.

| Statistical methods
We used generalized least square (GLS) that allows errors to be correlated and to have unequal variances. We tested for temporal autocorrelation for each wader species building two GLS,  We estimated effect sizes as Pearson's product-moment correlation coefficients by using standard conversions (Rosenthal, 1994).
These effect size analyses only included few observations, implying that the statistical power of any specific analysis is low. We adopted Cohen's (1988)

| Effect size, environmental change, and species at Tipperne during 1928-2014
Overall effect size weighted by (N-3) was on average +0.033

| D ISCUSS I ON
The main findings of this long-term study of population trends of breeding waders at two nature reserves in Denmark since 1928 and 1978 were significant impacts of multiple components of environmental change. In the present study, we tested for consistency in effect sizes for environmental variables hypothesized to affect population trends of waders. We focused on a suite of environmental change parameters hypothesized to act on breeding wader populations, although these species are migrants that spend the nonbreeding season along the East Atlantic Flyway from the Wadden Sea in the north to West Africa in the south (Bønløkke et al., 2006). The long-term time series dating back to 1928 allowed us to test for heterogeneity in strength of the relationship between abundance of breeding waders and multiple components of environmental change.
In particular, we were able to rank environmental components in terms of importance. We found no significant difference among species in effect size, but we documented significant heterogeneity among environmental factors, and these effects varied among species. Importantly, effect sizes for the two short time series at Tipperne and Vejlerne were positively correlated, and that was also the case when relating effect sizes for the short term and the long term at Tipperne. Thus, effect sizes for environmental factors were consistent across temporal and spatial scales.  (Dunn & Møller, 2014;Stephens et al., 2016). Arrival date and early breeding in waders are clearly affected by warmer temperature in spring, although altered by agricultural practice (Petersen, Meltofte, & Tøttrup, 2012;Schroeder et al., 2012). We showed considerable fluctuations in breeding populations of waders at Tipperne since 1928, explained by spring temperature and in particular precipitation. We documented a mean effect size of +0.197 (SE = 0.040) for spring precipitation and a weaker effect size of +0.110 (0.044) for spring temperature. Since both temperature and precipitation have increased, this implies that the changes in climate are those that improved the abundance of breeding waders the most. Temperature and precipitation are known to affect reproduction in waders (Schroeder et al., 2012), and populations responding positively to climate change are likely to increase (Møller, Rubolini, & Lehikoinen, 2008;Stephens et al., 2016).
Land use has changed consistently in the two study sites due to management. Interestingly, we had detailed information on the area grazed and therefore on its relative importance for breeding waders.
Grazing reduced the height of the vegetation, slowed down or even reversed successional processes, and increased arthropod biomass, which in turn had beneficial effects on growth of young (Norris et al., 1998;Eglington et al., 2008;Maier, 2013). In addition, vegetation height affects the ability of waders to observe predators at a distance, but also prevents use of suitable nesting sites and access to preferred foraging habitats for young due to tall swards (Cramp, 1985;Kleijn et al., 2010). We found evidence of a weak mean effect of the number of cattle on population size of different species of waders at the two study sites. However, the weak mean effect of number of cattle of −0.032 (0.026) implies that this management tool in fact had a detrimental effect rather than a beneficial effect on the number of breeding waders. In contrast, the area grazed had a mean effect of +0.031 (0.030). This implies that the number of breeding waders improved marginally with the area grazed by cattle.
We analyzed the effects of foxes on population size of breeding waders that mainly act through effects on nest predation and to a smaller extent on predation on adult birds (Beintema & Müskens, 1987;Meisner et al., 2014). We expected that foxes would negatively impact population trends of waders. Indeed, we found an expected mean effect of −0.106 (0.050). A total of 16 There was a negative impact of foxes on waders, as shown by Roodbergen et al. (2012).
Fertilizer increases nutrient availability, primary productivity, and subsequent effects on the abundance of animals at higher trophic levels in the marine environment (Phillippart et al., 2007;.  (Petersen et al., 2008).
This study has significant future prospects. First, we only analyzed the main factors that most likely affect populations and population trends of breeding waders. Clearly, it would be interesting to assess to which extent interactions between factors may impact populations and population trends. Second, this study has important implications for conservation in terms of management of nature reserves, management of populations of predators such as foxes, and management of vegetation as affected by grazing.
Clearly, most nature reserves, often small in size, will be impacted by a number of factors related to environmental change, but also influenced by surrounding areas that are much larger. We have shown here that effect sizes for short-and long-term effects are positively correlated and that different factors affect the size of breeding wader populations.
In conclusion, we have analyzed unique long-term data on breeding populations of waders with the longest time series starting in 1928. When analyzing the relationship between the abundance of breeding waders and multiple components of environmental change, we found significant evidence of effects.
While there were positive correlations between effect sizes for short-term studies at different sites, or long-and short-term effect sizes at the same site, these correlations were relatively strong accounting for 10%-15% of the variance. These findings emphasize the importance of considering heterogeneity in future monitoring schemes.

ACK N OWLED G M ENTS
We thank Jette Poulsen Engholm, Environment Center Ringkøbing, for providing data for nutrients. O. Gordo provided constructive criticism. The study received financial support from Aage V. Jensen Naturfond. We declare no conflict of interests.

AUTH O R S CO NTR I B UTI O N
APM conceived the project; OT and HHN collected the data; APM and KL analyzed the data; KL, APM, OT, HHN, and TA wrote the manuscript.

DATA ACCE SS I B I LIT Y
We suggest to store the data at TreeBASE, if the paper is accepted.