Changes in timing of agricultural activities and breeding Godwits
During the last 25 years, Black-tailed Godwits hatched their chicks at approximately the same date, whereas first mowing and grazing dates advanced by approximately 15 days. Perhaps surprisingly, our results suggest that the advancement of farming activities could largely be explained by climate change rather than by agricultural intensification. In 2005, farmers cut or grazed their grasslands at the same temperature sum, and therefore the same developmental stage of the vegetation as in 1982, the first year of this study. This temperature sum was, however, reached significantly earlier in the year. A possible explanation for the lack of any evidence of an advance of agricultural activities not caused by climate change may lie in the fact that agriculture in the Netherlands was already very intensive in the 1980s. Fertilizer inputs have actually decreased by 20% since then (Kleijn et al. 2009a), although other aspects of intensification like drainage, reseeding of grassland, and technical improvement of mowing and harvesting gear have continued.
In contrast to the advancement in recent decades, the advancement of mowing dates prior to 1980 probably does reflect agricultural intensification, as it occurred during a period of stable spring climate (Fig. 2). Lowering of water tables and increased fertilizer application stimulated grass growth independently of weather and the switch from hay to silage making led to swards being cut at an earlier stage. These developments probably also enabled (through an increase in soil macrofauna as food for adults or earlier availability of nest cover) and/or forced (through selective losses of later-hatching eggs and chicks) Godwits to considerably advance their breeding period (Beintema et al. 1985).
It is unclear why Black-tailed Godwits did not continue to advance their laying date after the 1970s. Selection pressure favouring earlier breeding still exists given that late-laying Godwit pairs produce considerably fewer fledglings than early pairs (Roodbergen & Klok 2008). Furthermore, the date on which the first Lapwing Vanellus vanellus eggs of the season were found by egg collectors advanced by about 10 days in the second half of the 20th century (Both et al. 2005). This was linked to higher spring temperatures and higher winter rainfall (Both et al. 2005). It is unknown what cues Godwits use to start egg-laying and incubation. The spring increase in temperature and start of vegetation growth have continued to advance in recent decades and are therefore unlikely to have formed constraints, which suggests an inability of adults to advance their arrival from the wintering grounds (Both et al. 2005) or nutritive constraints in the pre-laying period (Högstedt 1974, Nager 2006) as possible causes. The scant data available indicate that arrival dates of Godwits in the Netherlands have advanced and then stabilized roughly in parallel with laying dates, and that the length of the pre-laying interval has not changed (Fig. 2a). Understanding the lack of response of Black-tailed Godwit phenology to environmental change therefore may require more information on their spring migration and on foraging and energetics during the pre-laying period.
The relationship between land-use intensity and quality of chick foraging habitat
This study used vegetation height at median hatching date and N input as proxies for land-use intensity. It is unclear how well these proxies capture the wide range of aspects that are affected by agricultural intensification. However, vegetation height before the first cut has the advantage over other indicators, in that it is the product of all the activities taken by the farmer to optimize grassland productivity and it is relevant from the perspective of a foraging Godwit chick. Nitrogen input is less directly related to vegetation productivity or chick foraging habitat, but is used in many studies as an indicator of land-use intensity (e.g. Herzog et al. 2006, Kleijn et al. 2009b), which allows us to compare our findings with these studies.
The relationship between arthropods and the land-use intensity indicators was dominated by the response of the Diptera, which made up between 43 and 52% of all arthropods. This is similar to the range found by Schekkerman and Beintema (2007), who used the same methods in Dutch wet grasslands in the 1990s. Their abundance may explain why Dipterans are the most frequently taken prey items by Godwit chicks (found in 94% of the faecal samples; Beintema et al. 1991) rather than there being a genuine preference for this insect order. Ground-dwelling Coleoptera are not considered to be important food items, as Godwit chicks generally take food items from the vegetation rather than from the ground, and the Coleopterans in our samples were mainly ground-dwelling taxa such as Carabidae and Staphylinidae. Combining the arthropod abundance data (Table 1) with chick foraging preferences therefore suggests that in Dutch grasslands, Diptera, Araneae and Hymenoptera are the most important groups for Black-tailed Godwit chicks in terms of food quantity.
Schekkerman and Beintema (2007) found a pronounced short-term decline in arthropod abundance when fields were cut, which is relevant to Godwit chicks, as the first cut increasingly overlaps with their hatching period. However, Godwit broods strongly prefer to stay in uncut fields and travel considerable distances to reach them (Schekkerman & Beintema 2007), and hence variation in food availability in uncut fields as measured in this study is highly relevant.
In such uncut grasslands we found that, when significant, the relationships between the abundance of different arthropod groups and our two indicator variables of land-use intensity were all positive. The relationships of vegetation height and fertilizer input with total arthropod abundance were, however, only marginally significant and the relationships with total arthropod dry weight were not statistically significant, suggesting that the impact of agricultural intensification on the total prey abundance of Godwit chicks was positive but not very pronounced. Effects of vegetation height and fertilizer input on mean body mass were generally negative, although only convincingly so for Araneae. This is in line with the findings of Siepel (1990) and Blake et al. (1994) who found declining arthropod body size with increasing management intensities in grasslands. More intensively managed grasslands therefore contain more, but slightly smaller, prey items.
The body size of prey items is important for Godwit chicks because it determines how efficiently they can forage. Arthropods with a body dry weight below 1 mg cannot be used profitably (Schekkerman & Boele 2009), particularly by older chicks, and Godwit chicks indeed seem to prefer large arthropods (Beintema et al. 1991). In the examined grasslands, only Coleoptera and some Lepidoptera (which were not analysed separately but were included in the analyses of the total of all orders) consisted of animals in this size class. The Coleoptera consisted mostly of Carabidae and Staphylinideae, which are rarely eaten by Godwit chicks (Beintema et al. 1991), whereas mean body weights of the most abundant orders (Diptera, Araneae and Hymenoptera) were all well below 1 mg. Illustrative of this is that about 80% of the Diptera consisted of very small individuals (< 3 mm). If this size distribution is representative for the other arthropod groups, it suggests that total arthropod abundance may be a poor predictor of habitat quality, as only a small proportion of the total arthropod abundance can be profitably used by Godwit chicks. Interestingly, the arthropod groups with large individuals (Coleoptera, Diptera > 7 mm body length) were not significantly related to land-use intensity indicators.
The effects of land-use intensity on the quality of foraging habitat of Black-tailed Godwit chicks is therefore probably unrelated to food abundance. This suggests that, similar to findings for Meadow Pipits Anthus pratensis in UK grasslands (Vandenberghe et al. 2009), accessibility and harvestability of food may be the key factors determining the quality of the foraging habitat of Godwit chicks. Foraging efficiency of many grassland birds decreases as vegetation height increases because of a reduction in forager mobility and prey detectability (Butler & Gillings 2004). In our study, a large proportion of the fields were characterized by vegetation with 50% cover at 30 cm or higher during the Godwit chick period (Fig. 3a). These fields may be very difficult to access by Godwit chicks, particularly when they are young, unless they have an open horizontal structure, which is usually the case only at low levels of land-use intensity. Furthermore, because vegetation height increases more rapidly than arthropod abundance, tall swards host lower densities of arthropods (Fig. 3b). From the perspective of Godwit chick foraging efficiency, fields with low or sparse vegetation will therefore be most suitable. In such fields, the energetic cost associated with foraging is lowest and prey items are easiest to detect because they are concentrated in a small volume of vegetation.
Over the last few decades, farming activities in the Netherlands advanced but Black-tailed Godwit hatching dates did not. Twenty-five years ago most Godwit chicks hatched well before the onset of mowing and grazing. Currently, the hatching peak occurs after most mowing activity has taken place. This has a number of important implications. First, it means that an increasing proportion of clutches and vulnerable 1–2-day-old chicks are exposed to mowing activities or grazing cattle. This may explain why losses of Godwit clutches caused by agricultural activities were 6.7 times higher in the late 1990s than in the late 1980s (Teunissen et al. 2005). Secondly, hatched chicks currently find themselves in landscapes that are largely devoid of their preferred foraging habitat: tall uncut grasslands. Schekkerman et al. (2009) showed that the predation hazard for Godwit chicks is higher in recently cut or grazed fields than in uncut grasslands. Thirdly, the vegetation on the remaining uncut fields is taller, denser and therefore less suitable for foraging at the time that chicks hatch. This study shows that arthropod abundance is little affected by the vegetation structure and suggests that before the first cut of the season, quality of the foraging habitat is primarily determined by the accessibility of the vegetation to chicks. The decline in availability and quality of preferred foraging habitat may explain why Godwit chicks are currently in poorer condition than in the 1980s and why reproductive success and especially chick survival have declined in this period (Schekkerman et al. 2008). Thus, climate change and the associated advance of the start of agricultural activities result in a cascade of changes to the chick-rearing habitat of Black-tailed Godwits that all adversely affect chick survival.