Identifying Predators of Eggs and Chicks of Lapwing Vanellus

Ibis (2008), 150 (Suppl. 1), 74–85

Blackwell PublishingIdentifying Ltd predators of eggs and chicks of Lapwing Vanellus vanellus and Black-tailed Godwit Limosa limosa in the Netherlands and the importance of predation on wader reproductive output

WOLF TEUNISSEN,1* HANS SCHEKKERMAN,2 FRANK WILLEMS1 & FRANK MAJOOR1 1SOVON Dutch Centre for Field Ornithology, Rijksstraatweg 178, 6573DG Beek-Ubbergen, The Netherlands 2Alterra, Wageningen University and Research Centre, PO Box 47, 6700 AA Wageningen, The Netherlands, and Dutch Centre for Avian Migration and Demography, Netherlands Institute of Ecology (NIOO-KNAW), PO Box 40, 6666 ZG Heteren, The Netherlands

Farmland bird populations in the Netherlands have shown an accelerating decline in recent years, despite extensive conservation efforts including reserves, agri-environment schemes and protection of nests by volunteers. Although agricultural intensification is the main cause underlying these declines, there is a growing concern that the ongoing decline of grassland- breeding shorebirds in recent years is caused or aggravated by increasing predation. Although Red Fox Vulpes vulpes and Carrion Crow Corvus corone are often accused of causing widespread breeding losses, and calls for management of these species are made, very few field data are available on the incidence of predation on grassland shorebirds and the relative importance of different predators. To obtain such data, we identified egg predators using temperature loggers and continuous video recordings of 792 clutches, and chick predators by radiotagging 662 chicks of Black-tailed Godwit Limosa limosa and Northern Lapwing Vanellus vanellus. In total, 22 species were identified as predators of eggs or chicks, of which Red Fox, Common Buzzard Buteo buteo, Grey Heron Ardea cinerea and Stoat Mustela erminea were the most frequent. Eggs were taken primarily by mammals and chicks more often by birds. There was great variation in predation levels and species involved in predation of clutches between sites and years, but less in chick predation. Hence, there was no correlation between predation levels on clutches and those on chicks within the same sites. In sites where more then 50% of clutches were lost to predation, however, nocturnal predators took the larger share. As temporal and spatial variation on a small scale significantly influences predation levels, a site-specific approach based on sound knowledge of the local situation will be more effective in reducing predation on farmland birds than general, country-wide measures. Calculations based on our data indicate that eliminating only one loss factor at a time will often not reverse a local population decline, and provide a strong argument for targeting several locally limiting factors simultaneously instead of focusing on mitigation of predation alone. Keywords: agricultural intensification, conservation biology, farmland birds, habitat management, reproduction.

Almost all waders breeding in European farmland that the main cause of this reduction lies in low have shown a decline in population size in the last breeding productivity especially due to agricultural few decades (Thorup 2006). It is generally accepted intensification (Beintema et al. 1997, Kruk et al. 1997, *Corresponding author. Vickery et al. 2001, Wilson et al. 2004, Schekkerman Email: [email protected] & Beintema 2007). In the Netherlands, agri-environment Conflict of interests: The authors declare no conflict of interests. schemes (AES; principal measure postponed mowing)

Predators of Lapwing and Black-tailed Godwit 75

and reserves (principal measures postponed mowing METHODS and higher water tables) have been widely introduced to promote breeding performance of farmland birds, Study sites but with varying results (Kleijn et al. 2001, Willems et al. 2004, Schekkerman et al. 2008a). In addition, Data on depredation of eggs were collected in 10 on a large part of Dutch farmland, clutches are study sites scattered through the Netherlands (Fig. 1; marked and protected from agricultural losses by Teunissen et al. 2005). Sites were selected to cover a almost 20 000 volunteers and farmers (Van Paassen wide range of predation rates (based on data from & Roetmeijer 2006). preceding years) with emphasis on sites with high Despite these efforts the farmland bird population predation losses. They were characterized by dairy has declined at an accelerating rate (Teunissen & grasslands, with relatively high abundance of Lapwings Soldaat 2006) triggering debate on whether agricultural (> 25 breeding pairs per 100 ha) and Black-tailed intensification is the sole cause for the decline. There Godwits (> 10 breeding pairs per 100 ha), or a mix is increasing concern (particularly among the large of grassland and arable land, with high numbers of group of volunteers and farmers) about the effect of Lapwings and few or no Godwits. In all sites volunteers predation on eggs and chicks on population size and searched for nests and protected them against whether predation negates the positive effects of agricultural losses when needed. protective measures. Although there is little evidence Data for only Black-tailed Godwit chicks were that predation losses of wader nests have increased collected in four additional sites where the effective- strongly in recent decades (about 0.5% annually; ness of a new AES for Godwits was studied (Fig. 1; Teunissen et al. 2005), this discussion is often Schekkerman et al. 2008a). The main purpose of this emotional as (some) volunteers are losing all ‘their’ AES was to create a mosaic of different types of clutches to predation, and hence focus strongly on grassland by postponing mowing dates or grazing by the magnitude of predation losses and the identity of cattle. Each site consisted of an experimental plot key predators. It is the belief of many people involved managed according to the AES and a nearby control in the protection of farmland birds that Red Foxes that was farmed conventionally. Vulpes vulpes and Carrion Crows Corvus corone are In two study sites, Arkemheen and Lange Rypen, we the primary predators, as suggested by Pienkowski expected low levels of predation based on observa- (1984) and Parr (1993). Experimental removal of tions in previous years by local volunteers, whereas Red Fox and Carrion Crow has, however, shown in all other sites much higher levels had been observed. variable results for the survival of Northern Lapwing In most cases volunteers assumed that either Red Vanellus vanellus clutches (Bolton et al. 2007): some Fox (Bontebok, IJsseldelta, Langezwaag, Noordmeer) sites showed an increase of clutch survival whilst other or Carrion Crow (Sudermarpolder) or both (Leende, sites showed reductions. This was partly explained Ruinen, Soest) were the main predators, as the by differences in predator densities among sites, but animals or their tracks were seen in the area. another possibility is that in those sites other predators were active. These predators may require different Identifying predators of eggs management techniques. So identification of key predators and quantifying their impact are not only Identifying predators of eggs is difficult, because in essential for objective debate but also for effective many cases the nest contents are removed completely management. (Green et al. 1987), although sometimes predators In this paper, we present nest survey and chick can be identified from bite marks on the eggs (Green radiotracking data for Lapwing and Black-tailed et al. 1987, Bellebaum & Boschert 2003). We used two Godwit Limosa limosa from 10 sites across the methods to identify predators of eggs. To distinguish Netherlands over 4 years in order to: (1) quantify between diurnally and nocturnally active predators the spatial and temporal variance in the frequency of we placed temperature loggers (Tinytag, Gemini nest and chick predation, (2) identify the range and Data) in 545 nests to record nest temperature every relative frequency of predators of wader nests and 3 min, enabling us to assess the time of a predation chicks, (3) explore the variation across sites in nest event from the sudden substantial drop of nest predator species, and (4) explore the relative impact temperature followed by the nest tracking environ- of different causes of nest and chick loss on overall mental temperature as a consequence of the incubating fledging success. bird permanently leaving the nest (Fig. 2). The thermal

76 W. Teunissen et al.

Figure 1. Study sites where data were collected to determine the identity of predators of eggs (predation study) and chicks (predation and agri-environment scheme (AES) studies). Background shaded areas show relative predation levels in farmland in 2000 based on data collected by volunteers from 90 000 clutches (Teunissen et al. 2005). Darker shading indicates higher predation rates. probe was placed between the eggs and the logger predicted by ﬂoating eggs in water; Van Paassen et al. was buried beside the nest. Secondly, 247 nests at six 1984), and (2) if after the expected hatching date no sites were continuously recorded with infrared video small eggshell fragments were found in the nest, cameras (black-and-white bullet camera) with a indicating hatching. In all of these cases videotapes VHS time-lapse recorder (Sanyo time lapse TLS- were examined to identify the predator. In four of 1960) set to record one frame per second. The the six camera-sites Red Foxes were expected to be camera was placed on a metal stick, resembling those the main predators based on impressions by volunteers used by volunteers to mark nests, at a height of 1m and in preceding years. 3 m from the nest. Loggers stored up to 9812 days of data and nests were revisited every 4–10 days to Identifying predators of chicks check their status. At videotaped nests, tapes and batteries where replaced every 4 days. There were In total, 297 chicks of Lapwing (seven sites) and 365 two ways to distinguish predation of eggs: (1) if eggs of Black-tailed Godwit (12 sites) were radiotagged disappeared prematurely (hatching dates were (Schekkerman et al. 2008b). We used small 153-MHz

Predators of Lapwing and Black-tailed Godwit 77

Figure 2. Example of temperature recordings logged from a Lapwing clutch. When the bird is incubating the temperature in the nest is 39 °C. Temperature drops indicate times (logging was set to every 3 min) when the breeding bird has left the nest. This nest was left permanently on 4 June at 01:36 h and was predated. All nests that were predated between 20 min after dusk and 20 min before dawn were categorized as predated by nocturnally active predators.

VHF transmitters (type LB-2, Holohil, Canada, Tagged chicks were relocated every 1–5 days using assembled by Microtes, the Netherlands), weighing hand-held receivers (Icom America, USA) and 1.0 g and measuring 5 × 10 × 3 mm with a 12-cm antennas (Microtes). Whether the chicks were alive whip antenna and a battery life of ≥ 40 days. Chicks was deduced from their parents’ alarm behaviour were tagged within a day after hatching (86% of in combination with fluctuations in the strength of Godwits and 32% of Lapwings) or at older ages. their radio signal, indicating movement. Searches for Average hatching weight of Lapwing and Black-tailed missing chicks were made throughout the study area Godwit chicks was 17.5 and 28.5 g, respectively. and surrounding fields, focusing on scrub and wood- Preferably two chicks were tagged in broods of four, land up to several kilometres away which could hold one or two in broods of three with the remaining potential predators. Before the expected expiry date chicks ringed only. Transmitters were glued to a of the transmitter the whole study area was carefully 1.5 × 1.5-cm piece of cloth with superglue, and the examined for weak signals from transmitters in cloth was attached to the down on the chick’s back ditches or underground. with non-allergenic flexible latex-based glue (Uhu- After relocation of a dead chick or the transmitter, creativ, Uhu, Germany). Tagged chicks (and sometimes the cause of death was deduced (Table 1). In most their brood mates) were captured every 4–7 days to cases the location was informative (e.g. chick in restore the tag attachment, which deteriorated over ditch, between the grass on a recently cut field, time due to detachment of down and growth of under or in a raptor’s nest or plucking tree, in a Stoat underlying feathers. Mustela erminea burrow), but the state of the carcass

78 W. Teunissen et al.

Table 1. Characteristic locations and circumstances of dead chicks used to determine their fates.

Fate Locations and circumstances

Agricultural mowing/trampling chicks among recently cut grass; injuries such as missing legs or wings Ditch chick found in dry or wet ditch without injuries (beware that detached transmitters in wet ditches may result from Grey Herons soaking chicks before swallowing) Other no predation no visible injuries or location suggesting predation starvation no injuries, mass 40–60% of value expected at chick age predation adult predated remains of (marked) adult found Predation unknown Site (chick moved) or injuries suggest predation but not specific enough to suggest species Predation by bird bird transmitter at plucking site, feathers torn out, not bitten, antenna bent sharply (by bill) Marsh Harrier transmitter in nest Common Buzzard transmitter or ring under or in nest or plucking tree, signal from nest, in one case from bird Northern Goshawk ring in nest Common Jackdaw freshly predated, Jackdaws present at site and seen trying to catch chicks Carrion Crow antenna bent, ring or transmitter only, detached from carcass, found at plucking site Gull sp. ring or transmitter found in pellet, ring or transmitter in field with many gull tracks White Stork transmitter in nest, transmitter in pellet Grey Heron transmitter or ring found in colony; transmitter (detached) in or close to ditch Eurasian Sparrowhawk transmitter at plucking site Common Kestrel ring or transmitter in nestbox Predation by mammal mammal tooth bite marks, head or other body parts missing, carcass in site not readily accessible to bird Stoat/Weasel ring or transmitter in burrow (often in tunnel of European Mole) Domestic Cat transmitter found in farm courtyard Brown Rat transmitter in ditch side near farm, known to be inhabited by Rats Red Fox transmitter in burrow, transmitter found near burrow, bite marks on chick or transmitter

(condition, bite or plucking marks) and even of the U)] × L × K, where U = the probability that a clutch transmitter (antenna bent when torn off by a bird) survives to hatching, V = the probability that a failed conveyed information as well. Nevertheless, several clutch is replaced (taken as 0.5 for Godwits based on cases had to be left as ‘unknown’, ‘eaten by bird’, ‘not Schekkerman and Müskens (2000) and for Lapwings eaten’, etc. as 0.9 after their first clutch and 0.5 after their second Part of the registered predation will in fact be one (Van Balen 1959)), L = the number of eggs scavenging, for instance after mowing or other hatched per successful clutch and K = the probability agricultural activities. We could not distinguish that a chick survives to fledging. In this formula U is scavenging from predation based on chick and tag the product of the probability for each loss factor of remains. However, by comparing the predation rates clutches and K is the product of the probability for for intervals during mowing with intervals without each loss factor of chicks. We quantified the relative mowing, we found that the number of chicks predated importance of different loss factors of Lapwings and was slightly higher after mowing, suggesting that some Godwits by combining all observed rates in this scavenging did occur (Schekkerman et al. 2008b). formula and then excluding each factor one by one by setting the daily survival rate for that factor to one. Although survival of chicks will change with their Assessing the relative importance of age, we used the average daily survival rate for chicks different causes of nest and chick loss in these calculations. The results are therefore no To calculate overall fledging success (B, number of more than an indication of the impact that various fledged young per breeding pair) we combined data losses may have on overall fledging success. These on hatching success of nests in the study area with an calculations could only be made for the study sites of estimate of chick survival in a sample of radiotagged the predation study where we used temperature chicks. These are combined as: B = U × [1 + V × (1 – loggers or cameras and transmitters.

Predators of Lapwing and Black-tailed Godwit 79

Figure 3. Fate of clutches (based on daily survival rates with species data combined) monitored by temperature loggers and/or video cameras in each study site and year. Agricultural and unknown losses were combined in the category ‘other’. Numbers of nests examined in each site/year combination are given to the right side of the graph.

to weather and finally some chicks died of unknown RESULTS causes. In two cases one or both parents were killed by a Goshawk Accipiter gentilis, and hence the chicks Frequency of nest and chick predation did not survive. One Godwit chick was lethally Hatching success based on daily survival rates injured when it was attacked by an adult during an (binomial logistic regression; Aebischer 1999) varied interaction with another family. strongly between sites and years (Fig. 3). About 80% of the variation in hatching success was explained by Predators of wader nests and chicks predation losses (F1,39 = 145, P < 0.001). Predation losses varied between sites (F10,771 = 18.31, P < 0.001) Both diurnal and nocturnal predation rates on nests and years (F3,771 = 25.35, P < 0.001). For instance in differed between sites/year combinations (diurnal: 2002 predation rates varied from 8% (Arkemheen) F15,750 = 18.15, P < 0.001; nocturnal: F15,764 = 28.72, to 80% (Noordmeer) and in Arkemheen from 8% P < 0.001). Within sites, both overall predation (2002) to 51% (2004). rate and the proportion nocturnal/diurnal predation In 40% of all cases where chicks did not fledge, often varied between years and even between species their fate was unknown (Table 2). In most of these within years. Nevertheless, when data for both species cases the chicks were missing (tag not found and no were combined, there was a non-linear relationship signal received; Godwit 28%, Lapwing 37%). These between total predation (sum of diurnal and nocturnal chicks might have actually survived but observations predation) and diurnal predation within sites (linear in Godwit broods where we also tagged one parent term: F1,14 = 0.33, P = 0.57; quadratic term: F1,14 = showed that all missing chicks were dead, as parents 6.99, P = 0.01; R2 = 46.1%) and between total stopped their alarm display before the chicks could predation losses and nocturnal predation losses have fledged (Schekkerman et al. 2008b). Of the (linear term: F1,14 = 115.33, P < 0.001; quadratic term: 2 known losses 65% (Godwit) and 74% (Lapwing) F1,14 = 257.92, P < 0.001; R = 94.4%). In sites with were due to predation. Other losses were the result total predation losses ≤ 50%, both diurnal and of agricultural activities such as mowing (Godwit) or nocturnal predators were involved, whereas in sites drowning in ditches (primarily Lapwings). A small where total predation losses exceeded 50% this was proportion of chicks died of starvation or exposure primarily a consequence of nocturnal predators

Table 2. Species identiﬁed as predators of chicks and/or eggs of Northern Lapwings and Black-tailed Godwits. For each predator the number of chicks or clutches is given. Chicks from the same brood are treated as separate cases. No distinction is made between clutches that are fully or partially eaten. In parentheses are the proportion of chicks or clutches eaten of the total number of the two species. Data collected with cameras (clutches) and transmitters (chicks).

Chicks Clutches

Lapwing Godwit Total Lapwing Godwit Total

Predator unknown 19 (17.9) 16 (10.8) 35 (13.8) 10 (8.9) 2 (13.3) 12 (9.4) Mammal: identity unknown 2 (1.9) 11 (7.4) 13 (5.1) 0 (0.0) 0 (0.0) 0 (0.0) Hedgehog 0 (0.0) 0 (0.0) 0 (0.0) 1 (0.9) 1 (6.7) 2 (1.6) Brown Rat 1 (0.9) 4 (2.7) 5 (2.0) 0 (0.0) 0 (0.0) 0 (0.0) Stoat 20 (17.9) 6 (40.0) 26 (20.5) Stoat/Weasel/Polecat 9 (8.5) 30 (20.3) 39 (15.4) Polecat 0 (0.0) 0 (0.0) 0 (0.0) 1 (0.9) 0 (0.0) 1 (0.8) Beech Marten 0 (0.0) 0 (0.0) 0 (0.0) 3 (2.7) 0 (0.0) 3 (2.4) Red Fox 3 (2.8) 3 (2.0) 6 (2.4) 67 (59.8) 6 (40.0) 73 (57.5) Domestic Dog 0 (0.0) 0 (0.0) 0 (0.0) 1 (0.9) 0 (0.0) 1 (0.8) Domestic Cat 0 (0.0) 1 (0.7) 1 (0.4) 0 (0.0) 0 (0.0) 0 (0.0) Bird: identity unknown 23 (21.7) 21 (14.2) 44 (17.3) 0 (0.0) 0 (0.0) 0 (0.0) White Stork 0 (0.0) 2 (1.4) 2 (0.8) 0 (0.0) 0 (0.0) 0 (0.0) Grey Heron 13 (12.3) 7 (4.7) 20 (7.9) 0 (0.0) 0 (0.0) 0 (0.0) Tag in ditch; Grey Heron? 15 (14.2) 10 (6.8) 25 (9.8) Marsh Harrier 0 (0.0) 1 (0.7) 1 (0.4) 2 (1.8) 0 (0.0) 2 (1.6) Northern Goshawk 1 (0.9) 0 (0.0) 1 (0.4) 1 (0.9) 0 (0.0) 1 (0.8) Eurasian Sparrowhawk 2 (1.9) 0 (0.0) 2 (0.8) 0 (0.0) 0 (0.0) 0 (0.0) Common Buzzard 6 (5.7) 25 (16.9) 31 (12.2) 0 (0.0) 0 (0.0) 0 (0.0) Common Kestrel 0 (0.0) 5 (3.4) 5 (2.0) 0 (0.0) 0 (0.0) 0 (0.0) European Oystercatcher 0 (0.0) 0 (0.0) 0 (0.0) 1 (0.0) 0 (0.0) 1 (0.8) Black-tailed Godwit 0 (0.0) 1 (0.7) 1 (0.4) 1 (0.9) 0 (0.0) 1 (0.8) Common Gull 5 (4.7) 0 (0.0) 5 (2.0) 0 (0.0) 0 (0.0) 0 (0.0) Lesser Black-backed Gull 0 (0.0) 1 (0.7) 1 (0.4) 0 (0.0) 0 (0.0) 0 (0.0) Common Jackdaw 1 (0.9) 0 (0.0) 1 (0.4) 0 (0.0) 0 (0.0) 0 (0.0) Carrion Crow 6 (5.7) 10 (6.8) 16 (6.3) 5 (4.5) 0 (0.0) 5 (3.9) Eaten by bird 72 (82.8) 83 (62.9) 155 (70.8) 10 (8.8) 0 (0.0) 10 (8.6) Eaten by mammal 15 (17.2) 49 (37.1) 64 (29.2) 93 (91.2) 13 (100.0) 106 (91.4) Total 106 148 254 113 15 128

χ2 (Fig. 4). There was no difference between Lapwing (17 vs 6%, 1 = 6.30, P = 0.01), and both species were χ2 and Black-tailed Godwit in the relation between taken equally by Carrion Crows (7 vs 6%, 1 = 0.11, total predation losses and the proportion predated at P = 0.74). night (species added as factor to linear regression: F = 0.03, P = 0.864) or during the day (F = 0.62, 1,25 1,25 Variation across sites in nest predator P = 0.441). species In total, 15 predator species on chicks were identified (Table 2); 11 birds and four mammals. The On average 56% of the nests under camera surveillance most frequently identified predators were Stoats/ were predated, of which 93% was by mammals Weasels Mustela erminea/nivalis (15%), Buzzards (Fig. 5). Mammals were not exclusively active at Buteo buteo (12%), Grey Herons Ardea cinerea night: in Arkemheen all predation by Stoat, the only (18%) and Carrion Crows (6%). Other species each mammalian predator identified here, occurred during accounted for no more than 3% of the predation the day. Stoats from Lange Rypen predated three events. Grey Herons took Lapwing chicks more often nests during the day and one at night. The only other χ2 than Godwits (26 vs 13%, 1 = 7.90, P = 0.005), diurnally active mammalian predator in this study while Godwit chicks were taken more often by was a Domestic Dog Canis familiaris. Nocturnal χ2 Stoats (20 vs 9%, 1 = 5.49, P = 0.02) and Buzzards predators were: Beech Marten Martes foina, Polecat

identified, especially at Lange Rypen where at least five different species were recorded, including Red Fox, indicating that the presence of Red Foxes does not always lead to high predation levels. Of all known nest predation only 7% was attributable to birds, among which Carrion Crow, Goshawk and Marsh Harrier Circus aeruginosus (Table 2) were most frequent. Carrion Crow accounted for half of the avian predation. Predation events did not always include all eggs. Stoats took the entire clutch in 65.4% of all cases, Carrion Crow in 80% and Red Fox in 96%. Some predators collected one egg and returned to the nest after a few minutes or hours to collect the next egg. Sometimes it took several days before the predator Figure 4. Relationships between total predation loss of returned to the nest, particularly in the case of clutches (sum of diurnal and nocturnal predation) and losses by Stoats. One notable case was the predation by a dog: diurnal or nocturnal predation. Each dot represents a site/year combination. Lines indicate the non-linear relationship between at first it ate two eggs, 14 days later it ate the third total predation loss and nocturnal (solid line) and diurnal (broken egg and 5 days later the fourth egg hatched. line) predation losses. Impact on overall fledging success Martes putorius, Hedgehog Erinaceus europaeus and In Lapwings about half of the total reproductive Red Fox (Table 2). Red Foxes (59% of all predation losses occurred in the egg phase and the remainder events) and Stoats (19%) were identified most in the chick phase. In Black-tailed Godwits these frequently as egg predators, but the former might be losses were 35 and 65%, respectively. Predation expected as four sites were selected based on the accounted for 60% of all reproductive losses with a suspicion that Red Foxes were active there. In the known cause in Godwits and 75% in Lapwings. other two sites a wide variety of predators were Agricultural losses were limited, however, in all

Figure 5. Fate of failed clutches monitored by video cameras. The Arkemheen and Lange Rypen sites had average predation losses in the previous years. The other study sites were known to have high predation losses and Red Foxes were presumed to be the main cause. Due to technical problems with the equipment some predators remained unknown. Numbers on top of the graph indicate sample sizes. Mean observation time of camera nests was 9 days (range 1–30). Due to site selection overall hatching success was low (15% calculated from daily survival rates).

Figure 6. The relative importance of losses during breeding (egg) and fledging (chick) for Lapwing (upper graph) and Black-tailed Godwit (lower graph), respectively. ‘No exclusion’ represents reproductive output (fledged young) as observed in the study sites. The impact of each loss factor on reproductive output is examined by excluding that factor, i.e. by setting daily survival rate for that factor to one. Grey horizontal bars indicate the range of number of fledglings that should be produced to balance mortality of full-grown birds in order to sustain a constant population size.

study areas because of the occurrence of nest protec- ing success (Fig. 6). Only exclusion of predation of tion by volunteers. The variation in predation losses chicks by birds would lead to a substantial increase between sites was larger in the incubation phase than in overall fledging success (3.5 times higher). This in the chick phase (ranges: Godwit, incubation 0–75%, pattern was found in almost all study sites. At one chick phase 79–93%; Lapwing, incubation 27–87%, site (Leende), where several loss factors had a large chick phase 72–99%). As eggs are more often eaten impact on overall fledging success, no single exclu- by mammals than chicks this may be due to avian sion led to an increase. Exclusion of predation by predators being more evenly spread throughout the birds on chicks would on average lead to a higher landscape, as a result either of a more even breeding overall fledging success in Godwits as well (2.4 times distribution or of a larger activity radius. Hence we higher), but not as prominently as in Lapwings, did not find a relationship between the predation probably because there was more variation in the rates on eggs and chicks within the same areas dominant loss factor between sites. In one area 2 (Lapwing: F1,8 = 1.41, P = 0.28, R = 19%; Godwit: exclusion of predation by birds on chicks would 2 F1,14 = 1.92, P = 0.19, R = 14%). lead to a substantial increase, while in another site In Lapwings, if one of the loss factors is excluded exclusion of predation by mammals on chicks would during the egg phase it hardly affected overall fledg- do the same.

DISCUSSION Identifying predators Several of our study sites were selected for high Patterns in predation and predators predation losses of clutches in the past, in order to involved increase sample sizes for identification of predators. This study demonstrates that the eggs of grassland This pertained especially to sites where cameras waders were primarily eaten by mammals (93%) and were used (in four out of six sites predation losses their chicks by birds (71%, Table 2). Similar results were high in preceding years). These sites are therefore were found by Langgemach and Bellebaum (2005) not representative for the Netherlands as a whole and Bolton et al. (2007). In total, 21 predators of and average predation losses of clutches (46%) in our eggs and chicks were identified. Eggs were primarily study sites were higher than the national mean taken by Red Foxes and Stoats, although the two (27%; Teunissen et al. 2005). However, data on predators were rarely found together in the same chick predators were not only collected in the sites sites (Red Foxes are known to kill Stoats; Mulder where we identified egg predators but also in eight 1990). Other mammals took only a small number of other sites that were monitored in a study into the clutches. The main predators of chicks were Buzzards, effectiveness of a new AES for Black-tailed Godwits. Grey Herons and to some extent Carrion Crows. We found no difference in the proportion of chicks The only mammal that evidently took a substantial eaten by birds and mammals in the two groups of number of chicks was Stoat. sites (Teunissen et al. 2005, Schekkerman et al. Not only did we find a large variation in species 2008b), while the sites from the second study were composition of predators, but predation levels varied all selected in core areas for farmland birds in the greatly between sites and years as well. The only Netherlands. Moreover, levels of chick predation generalization supported by our data is that in areas were unrelated to rates of clutch predation in the with more than 50% loss of clutches to predation, same sites. Therefore, the species involved and their nocturnal predators play the major role. relative importance at least in chick predation are Red Foxes and Carrion Crows were generally likely to be valid. Although radiotags might be more presumed to be the most important predators by likely to be destroyed or buried out of range by farmers, local volunteers involved in clutch protection mammalian than avian predators, such bias would and conservationists (cf. Bolton et al. 2007). The role have to be severe to explain the larger amount of of Red Foxes was confirmed in this study (for clutch bird-associated predation events, and we think that predation only), but Crows took only 4% of clutches the difference between avian and mammal predation and 6% of chicks. Locally, their impact may be larger accurately reflects egg predation. as some individuals seem to specialize in taking Predators such as Red Foxes may respond to clutches (Picozzi 1975, Salath 1987, Sonerud & human activities such as marking nests in the fields. Fjeld 1987). This may have been the case in our In Bontebok the daily survival rate was lower in nests study as well, as four out of five clutches predated by with a camera than in nests without (Z = 2.42, Carrion Crow were in Leende, all close to an occupied P < 0.05) and this may have been the case in Ruinen Crow nest, although Crows were common in all as well (Z = 1.42, P = 0.16). In Leende, however, study sites. nests with cameras seem to survive better than nests There were differences between sites in the pro- without (Z = 1.61, P = 0.11). Again, individual portion of chicks taken by specific predators, but differences in behaviour may influence the impact this variation does not explain the differences in the predators have at a local scale. share of different species in predation of Lapwing and Godwit chicks. It is most likely that this is Implications for conservation caused by behavioural differences between the two species, including their breeding phenology (Lapwing: The primary cause of the decline of farmland birds hatching peak mid to late April, Godwit: hatching is the intensification of land use by farmers (Beintema peak early to mid May) and preference of chick et al. 1997, Kruk et al. 1997, Vickery et al. 2001). foraging habitat. Lapwings prefer short swards and This leads to a deterioration of the habitat, which in wet open ground where Herons often forage while turn may increase the extent of predation (Evans Godwits prefer tall grassland where Stoats can 2004) due to changes in the density of the breeding approach them unnoticed (Schekkerman et al. 2008b). birds or predators, and in the amount of cover where

nests or chicks can be concealed, or because breeding birds may be vulnerable to predation as well, and birds have to spend more time foraging – leaving the this would affect population dynamics relatively nest unattended – due to reduced food supply. Pre- strongly. A denser and more heterogeneous vegetation dation levels may increase as the density of farmland may improve nest crypsis and reduce nest predation birds decreases because they are less effective in rates but this may also impair anti-predator vigilance cooperatively excluding predators when nesting in for the incubating bird. In our study this may apply low densities (Green et al. 1990, Berg et al. 1992, to species such as Black-tailed Godwit and Common Seymour et al. 2003). Schekkerman et al. (2008b) Redshank Tringa totanus, which often conceal their showed that predation risk for Godwit chicks is several nests in tall vegetation. Our video recordings times higher when they stay in recently cut or grazed repeatedly showed that the breeding bird left the fields than in the uncut, tall swards which they pre- nest just in time (< 1 s) before it was predated, fer. Additionally, chick mortality can increase if food especially in case of predation by Stoats. However, availability is low as chicks will have to spend more in only one of the 145 recorded predation events time and take more risks in finding food. This can was the breeding adult killed (a Lapwing taken by a also lead to parents foraging at a larger distance from Red Fox). their chicks, which may slow down reactions to A major finding of our study is the large variation approaching predators. Finally, changes in densities between both sites and years in the overall level of of other prey owing to agricultural change can increase predation and the species involved, particularly in predation on farmland birds. For instance a drop in predation of clutches but to a lesser extent also in Common Vole Microtus arvalis density can increase chick predation. This suggests that predation levels predation by Weasels on farmland passerines (Evans are influenced by temporal or spatial processes on a 2004). small scale, for example the yearly presence or absence Eliminating predators as a conservation measure or location of activity ranges of specific (individual) may not always have the desired effect. Bolton et al. predators and the availability of alternative prey. In (2007) showed that removing Red Foxes and Carrion view of this heterogeneity, a site-specific approach Crows in the breeding season does not always lead to based on sound knowledge of the local situation will an increase in hatching success, especially in sites probably be more effective in reducing predation where predation levels were already low. Removing pressure on farmland birds than general, country- Carrion Crows or, in some areas, Red Foxes would wide measures. Our calculations show that eliminating not change much of the overall predation losses in only one loss factor, even if possible, will often not our study sites and it may even increase the number reverse local population decline. This provides a strong of some predators which avoid sites with Red Foxes argument for an approach targeting several locally present. Therefore, further research into relationships limiting factors simultaneously instead of focusing between habitat quality and predation is needed. on predation only. Our calculations on virtual exclusion of loss factors indicated that eliminating nocturnal predation on The work presented in this paper was supported by: clutches would not change the reproduction of Natuurmonumenten, Staatsbosbeheer, the Union of Lapwing or Black-tailed Godwits in an effective way Dutch Landscapes, Birdlife Netherlands, Landschapsbeheer in many sites. Only the elimination of avian predation Nederland, the provinces of Drenthe, Flevoland, Fryslan, on chicks could lead to a breeding productivity Gelderland, Noord-Holland, Noord-Brabant, Overijssel sufficient for the population to sustain itself (given and Zeeland, the Dutch Ministry of Agriculture, Nature Management and Food Quality, and the Postcode Loterij. current estimates for survival and age at first reproduc- Fieldwork was conducted by: L. van den Bergh, L. Beskers, tion for Black-tailed Godwits (Beintema & Drost 1986, K. Bouwman, S. Deuzeman, I. Geelen, P. Heemskerk, Groen & Hemerik 2002), the required productivity Y. van der Heide, B. Henstra, H. de Jong, M. de Jong, A. van level is approximately 0.6 fledged young per breed- Kleunen, M. Kuiper, F. Majoor, G. Müskens, W. Nell, ing pair), but this would be particularly difficult to R. Oosterhuis, H-J. Ottens, K-P. Plas, T. Meijer, E. Vromans, achieve by management. In most areas, however, several F. Weijdema and F. Willems. Numerous farmers and factors had to be excluded simultaneously to stabilize volunteers in the study areas provided assistance by estab- lishing contacts, access to land, finding and monitoring the population. In some cases eliminating all losses other nests and in many other ways. Mark Bolton helped with than predation also enabled populations to stabilize. the English text. We would also like to thank Jenny Gill, Our calculations assumed that predation affects James Reynolds and two anonymous referees for constructive reproductive success only, but the incubating adult comments on the manuscript.

investigator disturbance, nest cover and predator learning. REFERENCES Ardea 75: 221–229. Schekkerman, H. & Müskens, G. 2000. Produceren Grutto’s Aebischer, N.J. 1999. Multi-way comparisons and generalized Limosa limosa in agrarisch grasland voldoende jongen voor linear models of nest success: extensions of the Mayfield een duurzame populatie? Limosa 73: 121–134. method. Bird Study 46: 22–31. Schekkerman, H. & Beintema, A.J. 2007. Abundance of inver- Beintema, A.J. & Drost, N. 1986. Migration of the Black-tailed tebrates and foraging success of black-tailed godwit (Limosa Godwit. Gerfaut 76: 37–62. limosa) chicks in relation to agricultural grassland manage- Beintema, A.J., Dunn, E. & Stroud, D. 1997. Birds and wet ment. Ardea 95: 39–54. grasslands. In Pain, D.J. & Pienkowski, M.D. (eds) Farming Schekkerman, H., Teunissen, W. & Oosterveld, E. 2008a. The and Birds in Europe: the Common Agricultural Policy and its effect of ‘mosaic management’ on the demography of Black- Implications for Bird Conservation: 269–296. San Diego: tailed Godwit Limosa limosa on farmland. J. Appl. Ecol. 45: Academic Press. 1067–1075. Bellebaum, J. & Boschert, M. 2003. Bestimmung von Predatoren Schekkerman, H., Teunissen, W. & Oosterveld, E. 2008b. an Nestern von Wiesenlimikolen. Vogelwelt 124: 83–91. Using radiotelemetry to measure chick mortality and breeding Berg, A., Lindberg, T. & Kallebrink, K.G. 1992. Hatching success output in a precocial shorebird, the Black-tailed Godwit. of lapwings on farmland: differences between habitats and J. Ornithol., in press. DOI: 10.1007/s.10336-008-0328-4 colonies of different sizes. J. Anim. Ecol. 61: 469–476. Seymour, A., Harris, S., Ralston, C. & White, P.C.L. 2003. Bolton, M., Tyler, G., Smith, K. & Bamford, R. 2007. The Factors influencing the nesting success of Lapwings Vanellus impact of predator control on lapwing Vanellus vanellus vanellus and behaviour of Red Fox Vulpes vulpes in Lapwing breeding success on wet grassland nature reserves. J. Appl. nesting sites. Bird Study 50: 39–46. Ecol. 44: 534–544. Sonerud, G.A. & Fjeld, P.E. 1987. Long-term memory in egg Evans, K.L. 2004. The potential for interactions between predation predators: an experiment with a Hooded Crow. Ornis Scand. and habitat change to cause population declines of farmland 18: 323–325. birds. Ibis 146: 1–13. Teunissen, W., Schekkerman, H. & Willems, F. 2005. Predatie Green, R.E., Hawell, J. & Johnson, T.H. 1987. Identification of bij weidevogels, Report No. 2005/11, Beek-Ubbergen: predators of wader eggs from egg remains. Bird Study 34: SOVON Vogelonderzoek Nederland. 87–91. Teunissen, W.A. & Soldaat, L.L. 2006. Recente aantalson- Green, R.E., Hirons, G.J.M. & Kirby, J.S. 1990. The effective- twikkeling van weidevogels in Nederland. De Levende Natuur ness of nest defense by Black-tailed Godwits Limosa limosa. 107: 70–74. Ardea 78: 405–413. Thorup, O. 2006. Breeding Waders in Europe 2000. Interna- Groen, N.M. & Hemerik, L. 2002. Reproductive success and tional Wader Studies, Vol. 14. UK: International Wader Study survival of Black-tailed Godwits Limosa limosa in a declin- Group. ing local population in The Netherlands. Ardea 90: 239– Van Balen, J.H. 1959. Over de voortplanting van de Grutto. 248. Ardea 47: 76–86. Kleijn, D., Berendse, F., Smit, R. & Gilissen, N. 2001. Agri- Van Paassen, A. & Roetemeijer, W. 2006. Jaarverslag Weide- environment schemes do not effectively protect biodiversity vogelbescherming en –beheer in Nederland 2005. Utrecht: in Dutch agricultural landscapes. Nature 413: 723–725. Landschapsbeheer Nederland. Kruk, M., Noordervliet, M.A.W. & ter Keurs, W.J. 1997. Van Paassen, A.G., Veldman, D.H. & Beintema, A.J. 1984. A Survival of Black-tailed Godwit chicks Limosa limosa in simple device for determination of incubation stages in eggs. intensively exploited grassland areas in The Netherlands. Wildfowl 35: 173–178. Biol. Conserv. 80: 127–133. Vickery, J.A., Tallowin, J.R., Feber, R.E., Asteraki, E.J., Langgemach, T. & Bellebaum, J. 2005. Predation and the Atkinson, P.W., Fuller, R.J. & Brown, V.K. 2001. The conservation of ground-breeding birds in Germany. Vogelwelt management of lowland neutral grasslands in Britain: effects 126: 259–298. of agricultural practices on birds and their food resources. Mulder, J.L. 1990. The Stoat Mustela erminea in the Dutch dune J. Appl. Ecol. 38: 647–664. region, its local extinction, and a possible cause: the arrival Willems, F., Breeuwer, A., Foppen, R., Teunissen, W., Schek- of the Fox Vulpes vulpes. Lutra 33: 1–21. kerman, H., Goedhart, P., Kleijn, D. & Berendse, F. 2004. Parr, R. 1993. Nest predation and numbers of Golden Plovers Evaluatie Agrarisch Natuurbeheer: Effecten op Weidevogel- Pluvialis apricaria and other moorland waders. Bird Study 40: dichtheden. Report No. 2004/02, Beek-Ubbergen: SOVON 223–231. Vogelonderzoek Nederland. Picozzi, N. 1975. Crow predation on marked nests. J. Wildl. Wilson, A.M., Ausden, M. & Milsom, T.P. 2004. Changes in Manage. 39: 151–155. breeding wader populations on lowland wet grasslands Pienkowski, M.W. 1984. Breeding biology and population in England and Wales: causes and potential solutions. Ibis dynamics of ringed plovers Charadrius hiaticula in Britain 146 (Suppl. 2): 32–40. and Greenland: nest-predation as a possible factor limiting distribution and timing of breeding. J. Zool., Lond. 202: 83– 114. Received 13 March 2008; Salath, T. 1987. Crow predation on Coot eggs: effects of revision accepted 13 June 2008.