Earthworm availability in the Jura Mountains to the Eurasian Woodcock (Scolopax rusticola) during

the breeding season

Eurasian Woodcock (Scolopax rusticola) in Switzerland. Photo: Chris Venetz

Chris VENETZ

Swiss Ornithological Institute Supervisors:

Dr. Benjamin Homberger

Dr. Martin Grüebler

University of Neuchâtel Supervisors:

Professor-assistant Christophe Praz In Evolutive entomology laboratory

Senior lecturer Claire le Bayon In Functional ecology laboratory

Master Thesis in Biology

- 2 -

Table of Contents

Abstract ........................................................................................................................ - 3 -

1 INTRODUCTION ..................................................................................................... - 4 -

1.1 General background of the study .............................................................................. - 4 -

1.2 Focus of this study .................................................................................................... - 7 -

2 MATERIALS AND METHODS ................................................................................... - 8 -

2.1 Study Species ........................................................................................................... - 8 -

2.2 Study Area ............................................................................................................... - 9 -

2.3 Groundwork of the study........................................................................................ - 10 -

2.3.1 Capturing, radio tracking and home range definition ................................................. - 10 -

2.3.2 Woodcock’s food: qualitative approach ...................................................................... - 12 -

2.4 Study design........................................................................................................... - 14 -

2.5 Woodcock’s food: quantitative approach ................................................................ - 15 -

2.6 Environmental variables ......................................................................................... - 19 -

2.7 Data analysis .......................................................................................................... - 20 -

3 RESULTS .............................................................................................................. - 21 -

3.1 Faeces Analysis ...................................................................................................... - 21 -

3.2 Environmental variables likely to influence earthworm abundance ......................... - 22 -

3.3 Woodcock presence in relation to earthworm abundance ....................................... - 25 -

4 DISCUSSION ........................................................................................................ - 28 -

5 CONCLUSION ....................................................................................................... - 35 -

Acknowledgements .................................................................................................... - 37 -

Reference ................................................................................................................... - 38 -

- 3 -

Abstract

Breeding populations of the Eurasian Woodcock (Scolopax rusticola) in Switzerland

are declining for reasons poorly understood. Potential causes for the decline include

habitat change especially in regard to food and its abundance which was the primary

focus of this 1-year master thesis. According to the little literature about woodcock’s

food, the major part of the food composition consists of earthworms. Therefore,

confirming that earthworms can also be found in the food composition of woodcocks

in the Jura Mountains and then investigate their availability throughout woodcock’s

range are fundamental steps for understanding how food triggers habitat use of

woodcock in Switzerland. Based on a few fecal samples from trapped birds from the

Jura Mountains, a qualitative analysis under binocular was conducted and confirmed

presence of earthworm’s chaetae and thus importance of earthworms as a food

source. Assuming that earthworms are an important woodcock’s food, environmental

features correlated to earthworm abundance were then investigated. Results showed

that pH, soil humidity and soil texture were strongly correlated to earthworm

abundance while temperature was not significant. A seasonal pattern in earthworm

abundance was also observed which was likely related to earthworm life cycle traits.

Furthermore, another analysis demonstrated a strong relationship of earthworm

abundance with presence of woodcocks in the Jura Mountains. Earthworms might be

heterogeneously distributed within the soil and woodcocks spend much of their time

(probably actively feeding) where prey is available. This shows how important soil

characteristics allowing for high earthworm abundance are for woodcocks during the

breeding season. Conservations measures should aim at maintaining and creating

these ideal conditions to halt a further decline of the species in Switzerland.

- 4 -

1 INTRODUCTION

1.1 General background of the study

Nowadays, the importance of food availability as the mechanism driving habitat use

amongst birds is still controversial. In central Europe, home range size of

Tengmalm’s owl (Aegolius funereus) during breeding is determined by prey

abundance (Kouba et al. 2017). In contrast, the abundance of food resource for

forest passerines was not as important in determining habitat use in the temperate

subtropical region (Chaplin et al. 2009). The controversial topic has been a focus for

ornithologists for long time ago, especially when conservation perspectives are

discussed. One explanation to this could be that population decline of some species

can be caused by unavailable food resource. Ecological studies addressing such

questions are challenging since estimating and quantifying food abundance in a wide

area is a difficult and time consuming task. However, earthworm communities are

widespread and generally abundant in the soils and different methods are used to

estimate their population. The Eurasian Woodcock (Scolopax rusticola) tends to

prefer habitats with specific structure of herbaceous, shrubs and trees stratum in

Switzerland (Mollet 2015). However, it is yet poorly understood whether earthworm

availability is also a major habitat characteristic driving its spatial distribution. Hence,

still little is known about woodcock’s habitat characteristics and more work is needed

to understand how earthworm availability may impact woodcock’s population.

A few studies have addressed questions regarding abundance of earthworms

in Switzerland (Gobat et al. 2003; Ducommun 1989; Matthey et al. 1990; Cuendet et

al. 1997), but no research has yet focused on the Jura Mountains. Earthworms

constitute the highest biomass of soil macrofauna (Fragoso and Lavelle 1992), and

thus represent an important resource for several species of vertebrate’s predator

(Gobat et al. 2003). However, earthworms are known to be heterogeneously located

in hotspots (Rossi et al. 1997). Their distribution is related to the soil’s physical

characteristics and often represent an efficient indicator of pH, soil humidity, soil

structure and organic compounds (Gobat et al. 2003; Granval and Muys 1997;

Fragoso and Lavelle 1992). Their importance is shown in driving considerable

biological, chemical, physical process within the soil (Blouin et al. 2016; Salehi et al.

2013; Gobat et al. 2003; Jones et al. 1994). Therefore, they play a fundamental role

- 5 -

within every ecosystem they occur in by maintaining its biodiversity. As a

consequence, scarcity of earthworm habitats may seriously impact surrounding

species in the ecosystem, including associated predators like woodcocks.

Reportedly, the distribution and populations size of the woodcock in

Switzerland has declined in the last decades (Brüngger and Estoppey 2008; Mollet

2015; Knaus et al. 2018). The species disappeared from the Swiss Plateau and from

the eastern part of the Jura Mountains in the late 80’s (Mollet 2015; Brüngger and

Estoppey 2008; Schmid et al. 1998), while population in Bois du Jorat in canton of

Vaud went apparently extinct (Estoppey 2001a). In the Jura Mountains of the canton

of Neuchâtel, a study that intensively monitored woodcock’s population between

1998 and 2000 reported an evident desertion of several displaying sites. (Mulhouser

2002; Mulhouser 2001). These observations justify further investigation of factors

likely to affect breeding woodcock’s population. In 2015, the Swiss Ornithological

Institute published a synthesis that gathered current knowledge of the species, gave

conclusions and highlighted open questions regarding the state of the woodcock in

Switzerland (Mollet 2015). The synthesis discussed important factors such as hunting

pressure, disturbance or habitat change, especially in relation to food availability. The

change in food availability as a potential factor driving woodcock’s decline is yet

hardly understood and thus more work is needed in this thematic.

There are only few studies investigating food ecology of woodcocks during the

breeding period and investigating it is challenging. Ecological studies of the species

are difficult due to the secretive behavior. Watching a woodcock and identifying its

prey in the field is even more complex because woodcocks are constantly searching

for prey by probing the soil with their long beaks. The diversity of prey is hence little

explored. The anatomy of the bill defines the woodcock as a specialist predator of

soil macrofauna (Hirons and Bickford-Smith 1983; Whiterby et al. 1940; Steinfatt

1938). Previous studies typically investigated food items based on stomach content

from hunted birds (Granval 1988; Granval 1987). In France, based on dead

specimens, earthworms composed up to 90% of the stomach content (Granval 1988;

Hirons and Bickford-Smith 1983), representing the most important food for wintering

woodcocks (Granval and Muys 1992; Granval 1987). Other food items reported by

the same authors were soil arthropods such as Coleoptera, Dermaptera, Diptera,

Isopoda and Myriapoda (Granval 1987).

- 6 -

In one case, a recent study from the U.K fecal analysis was performed on

samples collected during breeding time and demonstrated a similar outcome to those

of wintering birds in France. In their analysis, earthworms, spiders and harvestmen

were detected, with earthworms depicting by far the most predominant food item in

terms of biomass (Hoodless and Hirons 2007). Other reports of faeces contents

include invertebrates such as beetles’ larvae, millipedes, woodlices, butterflies,

moths, sawflies larvae, ants and flies (Hoodless and Hirons 2007). Hence, according

to current knowledge, the woodcock must be regarded as an earthworm specialist

rather than a generalist invertebrate’s predator (Hirons and Johnson 1987; Granval

1987; Granval and Muys 1992). From Switzerland, there is only anecdotal

information on food of breeding woodcocks.

Little is known about the relation between earthworm availability and

woodcocks. Correlative studies on wintering grounds in France showed that

woodcock preferred grazed meadow habitat containing five times higher biomass of

earthworms compared to cultivated fields (Duriez et al. 2005). Less is known about

the food and its availability on the breeding grounds. As a single case in the Alps of

Switzerland, a study conducted in a small surface in the forest reserve of Amden

(canton of St. Gallen) revealed that woodcocks tend to select habitat with high

biomass of earthworm (Lanz 2008). Although this relation was exhaustive, it is

nonetheless difficult to separate woodcock presence and absence spots at such a

small surface without having support of precise telemetry locations. Moreover, the

importance of earthworm in the diet of the woodcock in the Swiss Alps has as yet not

been confirmed.

Interestingly, winter and spring habitats differ strongly, but the question of how

food items change between winter and spring has not yet been studied. If woodcocks

change their habitats during the year, they are likely to depend on different

invertebrate prey spectra between breeding and wintering grounds. Importantly, on

wintering grounds, woodcocks typically feed at night in the meadows which are the

richest habitat for earthworms (Edwards 1983), and probably because earthworms

emerge in higher abundance at night than during daylight (Duriez et al. 2005).

Conversely, in spring and during breeding time, woodcocks shift feeding to daytime

in the forest (Brüngger and Estoppey 2008). This change in feeding strategy raises

questions whether earthworms are as important as suspected for woodcocks

throughout the whole year.

- 7 -

1.2 Focus of this study

Fundamental knowledge of the habitat requirements and especially food availability

on the breeding grounds remain lacking and needs to be treated as a central

question if woodcock’s decline wants to understood. Hence, the Federal Office for

the Environment (FOEN), established in 2014 a national project in order to determine

reasons of the decline and develop some optimal conservation measures within the

breeding sites (Gonseth and Bohnenstengel, 2015). Upon request from this national

project and under supervision of the Swiss Ornithological Institute, the food and its

availability in the Jura Mountains were explored in this master study.

The general aim of this study was to clarify woodcock’s food and its

abundance in the Jura Mountains with a special focus on earthworms. I used a

correlative approach since experimental manipulations of food availability in the field

were hardly possible. I looked at abundance of earthworms in relation to

environmental variables likely important for earthworms and the presence of

woodcocks. I separated my analyses into several steps (Figure 1). Firstly, I

investigated qualitatively whether, similar to other study sites, earthworms are

important prey species of woodcocks during the breeding period. Therefore, I

observed under a microscope several faeces samples and looked for earthworm’s

chaetae. This step was needed to know what to sample in the field and how to

develop the field protocol. Secondly, I investigated how abiotic environmental factors

such as soil characteristics or date were related to earthworm abundance.

Importantly, the aim of the study was not to exhaustively determine the ecology of

earthworms in the Jura Mountains but to investigate their importance and relationship

to the woodcocks. Finally, I evaluated the probability of woodcock presence in

relation to earthworm abundance based on samples from within 10 different home

ranges and control sites outside home ranges.

I expected that earthworm abundance was an important food of woodcocks

during the breeding season. Furthermore, I expected that earthworm abundance was

driven by soil characteristics. Especially, humid soils should harbor high earthworm

abundance. While for pH, I expected a range of tolerance with an optimum in slightly

acidic soils. Air temperature was also expected to regulate earthworm presence.

- 8 -

Finally, I suspected the abundance of earthworm to be a potential driver of

woodcock’s distribution in the Jura Mountains.

Figure 1: Schema showing two important themes of this study: After confirming direct importance of earthworm in the diet under binocular, the first step was to determine environmental variables that influence the abundance of earthworms and secondly, the distribution of woodcocks in relations to earthworm abundance.

2 MATERIALS AND METHODS

2.1 Study Species

The Eurasian Woodcock (Scolopax rusticola Linné, 1758) belongs to shorebirds of

the order Charadriformes and to the family of Scolopacidae (Del Hoyo et al. 1996). It

is among the few species of shorebirds that are restricted to forest habitat during

breeding season (Ferrand and Gosmann 2009; Del Hoyo et al. 1996). It has an

extremely wide range throughout Eurasia, from Spain including the Acores, to the far-

eastern Asia in Japan and Sakhalin Island (Del Hoyo et al. 1996).

The Swiss breeding population is estimated between 1000-4000 breeding

pairs (Knaus et al. 2018). As a short distance migrating bird, woodcocks arrive on

breeding grounds between March and May and breed until end of August before the

autumn migration starts in October (Del Hoyo et al. 1996). In Switzerland, the

species mostly breeds in the western and central part of the Jura mountains, in the

northern part of the Alpine foothills, in the north of the Grison canton, and locally

throughout the central part of the Alps (Knaus et al. 2018; Maumary et al. 2007)

(Figure 2).

When studying woodcocks, challenges include estimation of the population

although methods and technology of monitoring have been remarkably improved in

the last decades (Knaus et al. 2018, Mulhauser and Zimmermann 2015; Mulhauser

and Zimmermann 2010b; Mulhauser and Zimmermann 2010a; Brüngger and

Estoppey 2008; Estoppey 2001b; Estoppey 2001a). The estimation of the breeding

- 9 -

population is based on counts of displaying males, while female sights remain rare or

even absent in some sites. (Mollet 2015; Ferrand and Gossmann 2009; Brüngger

and Estoppey 2008; Mulhauser 2001; Andris and Westermann 2002, Lauer et al.

2006; Estoppey 2001b; Tester and Watson 1973).

Figure 2: Distribution of the Eurasian Woodcock (Scolopax rusticola) in Switzerland between 2013 and 2016: Red squares show where woodcocks have been reported by the last Swiss Atlas of Breeding Birds 2013-2016. (Knaus et al. 2018).

2.2 Study Area

The fieldwork was conducted in the Jura Mountains in the canton of Neuchâtel and

across the border of canton of Vaud. More specifically, the study covered the region

of la Brévine NE in the northern part, the southern part was delineated from St-Croix

VD to Mauborget VD, and covered most of the region of Val-de-Travers from

Noiraigue NE to Butte NE and Les Verrières NE (308.5 Km2). The elevation of the

study area lay between 754m and 1508m. The landscape is mainly covered by forest

(51%) and agricultural land (42%). Around 6% is covered by settlement zone and

human infrastructure. Human population density in the region of Val-de-Travers and

- 10 -

the border of canton de Vaud is 86 citizens per km2 while in La Brévine NE it is 15

citizens per km2.

2.3 Groundwork of the study

2.3.1 Capturing, radio tracking and home range definition

My study was integrated into a bigger research project on the woodcock initiated by

the FOEN. In the framework of this project, woodcocks were captured during evening

display, measured and equipped with radio telemetry tags in the years 2016 and

2017 (Rocheteau et al. 2017). Thereafter, birds were followed by a telemetry team

and located at least every third day. Based on precise location (precision < 50 Meter)

of the birds, kernel home ranges of 10 woodcock males captured in 2017 were

calculated (Table 1). Home ranges are defined as the utilization distribution of the

animal that are regularly crossed during its activities of feeding, mating and caring for

young (Burt 1943). Woodcock’s home ranges were estimated using the Kernel

method (Worton 1989; Van Winkle 1975). Kernel calculations allow to separate home

ranges according to the usage density (Calenge 2006), Hence, we separated each

home range into their 30% (intense use), 60% (intermediate use) and 95% (low use)

sections (Figure 3). The sections are defined as the smallest possible areas

encompassing the respective percentage of telemetry localizations (Calenge 2006).

Table 1: Table of the 10 individuals including their area of homes-ranges. Ring numbers, age of the birds and dates of capture are also given.

- 11 -

Figure 3: Map of the study area showing a home range with the different usage densities (30% in purple, 60% in green and 95% in blue) of home range sections and earthworms sampling points in yellow

- 12 -

2.3.2 Woodcock’s food: qualitative approach

Before starting fieldwork, it was important to evaluate and confirm qualitatively what

food items can be found in faeces of woodcocks in the Jura Mountains. This step

would allow to develop the further sampling design and field protocols focusing on

the most relevant prey species.

To date, several methods were suggested to evaluate food composition of

birds such as behavioral observation, analysis of stomach contents, emetic

techniques, pellets and faeces analysis with a microscope or molecular methods

(Hartley 1948; Pienkowski et al. 1984; Duffy and Jackson 1986; Rosenberg and

Cooper 1990). Behavioral observations and pellets analysis are commonly used for

owls and raptors. In Switzerland, a recent observational study on the short-toed

snake-eagle (Circaetus gallicus) showed that food brought to the nest consist strictly

of viperidae (Maumary et al. 2013). Similarly, microchiropteran were confirmed in the

diet of little owl in England based on pellet defections (Athene noctua) (Hounsome et

al. 2004). Behavioral observations and pellets analysis are not suitable for

woodcocks owing to their secretive behavior (feeding on ground with beak in soil),

and since woodcocks do not regurgitate pellets. In France, analysis of stomach

contents of woodcocks is commonly used in specimens collected from hunting

activities. These analyses gave exhaustive results (see section 1.1; Granval1988;

Granval 1987). However, in Switzerland hunting is not allowed during the breeding

seasons, hence no stomach samples were available. It has been shown that emetic

techniques may provide more information about diet than pellets and fecal analysis

since stomach contents are less digested and easier to examine (Poulin and

Lefebvre 1995). However, emetic methods can provoke mortality among birds

(Rosenberg and Cooper. 1990) and were therefore not taken into consideration.

Analyzing food content from faeces is relatively convenient since samples can be

obtained relatively easy. A recent study provided evidence that fecal samples give

similar information than other methods. (Carlisle and Holberton 2006). However,

challenges and limitations of fecal analyses are set by the advanced digestion state

which has to be taken into account. Fecal samples can be either analyzed under

microscopes or by DNA-based methods (Oehm et al. 2017). DNA-based methods

are efficient but takes considerable time. Hence, analysis of fecal samples under

microscope is likely the most suitable and affordable method. In the U.K, analysis

- 13 -

under microscope of diet components of woodcocks based on fecal samples already

showed that it is an efficient method (Hoodless & Hirons 2008).

Faeces samples were thus collected when woodcocks were captured

(Rocheteau et al. 2015). More specifically, as soon as one individual was trapped,

the bird was put into a box containing a protected mesh, with a blotting paper at the

bottom to collect the faeces samples. Faeces samples were then tried and kept in a

freezer until analysis in the laboratory.

Digestive system of several species of birds are not able to decompose

earthworm’s chaetae which can be used to confirm earthworm presence in the food

(Wroot 1985; Paris 1914). Chaetae are chitinous epidermal structures found on

earthworms (Hausen 2005). Hirons (1978) revealed the presence of some

earthworm’s chaetae in the stomach of woodcocks wintering in France. More

recently, chaetae were also found in the faeces of the population in the U.K

(Hoodless and Hirons 2007).

Woodcocks are well adapted to feed on earthworms and I wanted to see

whether earthworm’s chaetae can also be found in the faeces from the Jura

Mountains collected during the breeding period. I also wanted to see whether

remnants of other prey can be found. Based on these results, I could then develop a

field sampling protocol. To analyze fecal content, I applied the same protocol

described by Hoodless and Hirons (2007) in their study. A total of five samples were

observed under a binocular. Faeces analysis was performed at the University of

Neuchâtel in the Functional Ecology Laboratory under permission of Professor

Sergio Rasman, while other examinations of chaetae under microscope were

performed in the Laboratory of Soil Biodiversity of the University of Neuchâtel. The

samples were stored in 70% ethanol and components of the faeces were separated

by size into three different sections with two sieves of 200µm and 50µm. According to

sieve sizes, larger earthworm’s chaetae are supposed to be found up to 200µm

(chaetae > 200µm), while small chaetae are normally detected between 200µm and

50µm (200µm > chaetae > 50µm) (Hoodless and Hirons 2007). If remnants of other

undigested prey were detected, they were also reported. Further investigation was

stopped after having collected a total 5 bristles from each of the 5 samples. Since

only few samples were investigated with this approach, no quantitative analysis was

performed.

- 14 -

2.4 Study design

In the field, I conducted earthworms sampling (hand sorting) in 10 home ranges as

described below. Each home range was subdivided into three sections in accordance

with the intensity of use (Kernel estimator of 30%, 60% and 95%). And each of these

sections include two different sites of sampling (2 sites x 3 sections), making a total

of six sites within each home range (Figure 4). These presence sites are distributed

over some of the telemetry localizations. In order to compare earthworm densities of

presence home ranges with pseudo-absence sites, I additionally sampled sites

outside of the home ranges. The pseudo-absence sites were randomly distributed

over the whole study area avoiding all known home ranges and sites that were

otherwise known to be occupied by woodcocks. In total, I subsampled 60 sites within

home ranges of 10 individuals and 40 pseudo absence sites outside of the home

range, making a total of 100 sites (Figure 5).

Only male woodcocks show active roding behavior (Ferrand & Gossmann

2009). Since we captured woodcocks during roding periods, we could only capture

and radio-track male woodcocks (Rocheteau et al. 2015). All my further analyses are

therefore based on males.

Figure 4: Experimental design representing a schematic home range with its surrounding absence sites. A home range was separated into three sections of usage density: 30% home range in red, 60% home range in orange, 95% home range in yellow. The absence section is in white.

- 15 -

Figure 5: Map showing the entire study area, including all sampling sites within the sections (30%, 60%, 95%) of the home ranges (n=60; red dots) and all absence sampling sites that have been studied (n=40; blue dots).

2.5 Woodcock’s food: quantitative approach

There are three methods commonly used to extract earthworms from soils. Firstly, a

lethal, and nowadays illegal method in Switzerland, involving formalin extraction to

provoke emergence of earthworms from the soil (Bouché and Aliaga 1986; Bouché

and Gardner 1984). Formalin is not only lethal for earthworms but it is also highly

toxic for nearby plants and soils (Eichinger et al. 2007). Formalin is also known to

pose considerable health risks to humans (IARC 1995; Fischer 1905). Hence, this

method was not applicable in this study. Secondly, a mixture of water and Allyl

Isothiocyanate (active compound of mustard) can be used to extract earthworms

from soils (Gunn 1992). Unlike formalin, this solution is apparently non-lethal for

earthworms and non-toxic to humans (Gunn 1992). However, the method needs high

amounts of water which makes it difficult to apply in challenging terrain. Moreover,

with both extraction methods, there is a risk that earthworms escape the extraction

and the quantification may be not precise. Finally, hand sorting is another method

that is considerably more accurate than extraction, although it takes considerable

time. As an example, in the U.K, hand sorting emerged 2.09x as many earthworms

- 16 -

as the formalin method (Hoodless and Hirons 2007). Moreover, hand sorting is a

simple method that does not need a lot of material. Given the advantages, I

developed a protocol for hand sorting as described below:

Earthworms are heterogeneously distributed in the soil (Rossi et al. 1997;

Poiter and Richter 1992). To consider this spatial distribution, it is often advised to

sample between 3-6 plots at one site (Lee 1985; Duriez et al. 2006). At each site, I

therefore sampled 5 plots (Figure 6). As a first step, the exact position of the site

was reached using a map. This exact position represented the central plot of

sampling. From this center plot, additional 4 sampling plots were defined in 20 m

distance north, east, south and west of the center plot. Each plot was defined by a

0.5cm x 0.5cm = 0.25m² square where hand sorting was performed.

Overall, a total of 500 plots in 60 presence sites (from 10 home ranges) and

40 pseudo-absence sites were dug for sampling earthworms. A shovel was used to

dig the soil. Only the top soil layer of 10 cm depth was sampled which corresponds to

the length of the woodcock’s bill. The extracted soil was carefully transferred onto a

tarpaulin (Figure 7a). Hand sorting was then performed by separating earthworms

from the mixture of the soil by hand (Figure 7b). Finally, earthworms were transferred

into a jar, they were counted and weighted (Figure 7c) and released into the same

plot. The volume of soil (0.5m x 0.5m x 0.1m = 0.025m3) dug per plot was maintained

the same whenever it was possible. If the terrain did not allow to dig this volume, the

effective volume dug was noted. It was also recorded if terrain conditions did not

allow digging at all. Thereafter, earthworm quantity was always indicated as

abundance, i.e. earthworm number divided by soil volume dug.

My earthworm sampling was restricted to daytime hours between 9:00 to

16:00 This was justified since woodcocks have been suggested to be active almost

exclusively during daytime in Switzerland (Brüngger Estoppey 2008). On the other

hand, earthworms show diurnal activity patterns emerging to the surface at dusk (Lee

1985) when woodcocks are busy roding. However, in our daytime sampling we found

reasonable worm densities which did not change considerably throughout the day.

Hence, our daytime sampling seems representative for worm densities actually

available to woodcocks. Also, digging was not conducted under harsh weather

conditions.

Sampling was randomized as good as possible. I visited one home range

(including its 6 sites) and 4 absences sites per week, making a total of 10 sites (50

- 17 -

plots). The 10 sites were randomly chosen during the week, but not the plots.

Alternating the plots would have been very time consuming (Table 2).

Field accommodation and material storage were in Fleurier NE. The Swiss

Ornithological Institute provided a car during the entire time of the fieldwork which

allowed to reach every sites in the study area.

Figure 7a Figure 7b Figure 7c

Photos showing the different steps of hand sorting: Figure 7a shows the soil mixture transferred onto a tarpaulin with the shovel; Figure 7b shows an earthworm separated from the soil mixture; Figure 7c shows earthworms transferred into a jar and ready for biomass measurements.

- 18 -

Figure 6: Representation of one site of 28 m2 which corresponds to one of the 10 home ranges.

Absence sites were treated equally. Within each site, there were 5 standardized plots of digging of 0.25m

2 with a depth of 10cm.

Table 2: Timetable indicating for each week which sites are due to be dug. Colors indicate sections within home ranges (red: 30%; orange: 60%; yellow: 95%) or absence sites (white). A mean of 2 sites (2x5 plots) were dug per day, five days per week.

- 19 -

2.6 Environmental variables

Distribution and abundance of earthworms in the Jura Mountains likely depend on

several key factors (Granval and Muys 1997). These presumably important factors

were measured on each site and are described below:

pH and soil humidity Previous studies showed that presence of earthworms is influenced by the soil pH

(Bhatti 1962; Bachelier 1978) An optimal pH was found for several species (Edwards

and Bohlen 1996). Most of the species usually occur between pH=5.0 and pH=7.4

(Satchell 1967). While several species have a tolerance to low pH, most earthworms

are generally absent from acidic soils (Curry 1998).

Soil humidity is a key physical characteristic for ensuring the survival and

activity of the earthworm’s community (Curry 1998, Satchell 1967, Gobat et al. 2003).

Similar to pH, an optimal range of soil humidity is expected. I used a high quality pH

and humidity meter developed for gardening (Kelway soil pH and moisture meter),

which can reliably measure soil pH down to the decimal unit and relative humidity

down to one percentage. The meter was put into the soil and results were obtained

within five minutes.

temperature Temperature can have an considerable effect on earthworm’s activity (Bouché 1972,

Satchell 1967). In response to very low temperature, earthworms are able to enter

into hibernation (Bouché 1972). Air temperature in Celsius C° degree was measured

using a digital thermometer (Hama model Xavax) at each site.

soil texture

Previous studies showed that earthworm presence increased with increasing clay

content. This suggests that physical structure of sandy soil is not favorable for

earthworm’s movement (Nordström and Rundgren 1974; Satchell 1967). Soil texture

analysis is done by an examination of size distribution of grains (Gobat et al. 2003).

Precise quantitative measurements of soil texture require a hydrometer method in the

laboratory which is time consuming. However, qualitative measurements in the field

by hand is commonly used for estimating soil texture. For such estimation, I followed

the protocol described by Gobat et al. (2003), which separate the soil texture in three

types: sandy soil, loamy soil and clay soil.

- 20 -

2.7 Data analysis

Microsoft Excel 2016 © version 2016 was used in order to record field data for later

analysis. I also used this program to calculate the total abundance and biomass per

unit volume of earthworms. To compute statistics and generate graphics, the free

software R (3.5.2) and Rstudio Version 1.1.456 – © 2009-2018 RStudio, Inc. were

used.

In a first step, all variables were checked for outliers using histograms, then

covariance between variables were calculated. Before modelling, all variables were

standardized so that effects sizes can be easily compared. Mixed-effects models

were then specified with two aims:

Modelling earthworm abundance in relation to environmental variables to

explore how abiotic environmental variables were associated with earthworm

abundance

Modelling woodcock presence in a binomial model in relation to earthworm

abundance to see whether woodcock presence/absence was associated with

earthworm abundance.

The 5 sampling plots within each sites were relatively close together which implied

spatial autocorrelation. I remedied this problem by included “site” as a random factor

in the mixed effects model. In both models, I included the following 7 variables: soil

humidity, pH, date, meteo, temperature, soil texture and day timing. To account for

unimodal effects (optima), I included 2nd order polynomials of the following variables:

Soil humidity, pH and date. I fitted a first model including all variables and then

backward eliminated the term showing the lowest significance in an iterative process

until only significant terms remained. For graphical representation of the results, I

predicted from the final models including only significant terms by generating

posterior distributions of all parameters of interest (Gelman & Hill, 2006).

To check whether earthworm abundance significantly differed between the

absence sites and the sections of the home ranges (30%, 60%, 95%), a linear model

was fitted describing earthworm abundance in relation the sections. Here again, I

controlled for spatial autocorrelation by including “site” as a random effect.

- 21 -

3 RESULTS

3.1 Faeces Analysis

Qualitative analysis under binocular confirmed presence of earthworm’s

chaetae (Figure 8) in the fecal samples. A total of 30 chaetae were found in 5

samples coming from 5 different individuals. This result highlighted the importance of

the earthworms in woodcock’s food in the Jura Mountains and justified the

development of a field protocol focusing specifically on earthworm abundance.

According to the sieve size, most earthworm’s chaetae were detected in sieve

up to 200 µm (chaetae > 200 µm) while fewer were found between 200 µm and 50

µm (200 µm > chaetae > 50 µm). No chaetae were detected under 50 µm (50 µm >

chaetae). Surprisingly, no other undigested fragments of soil macrofauna were

detected. A few fragments of plants were present but they were not identified.

Earthworm’s chaetae or other food items were not counted or quantitatively

analyzed.

Figure 8: A massive earthworm’s chaeta of 500 µm found in a faeces sample. The chaeta, is easily identifiable by the sigmoidal and clear appearance and the thicker structure in the middle. This bristle came from a sample that was collected on the individual captured on 12.05.2017 at La Rochetta NE.

- 22 -

3.2 Environmental variables likely to influence earthworm abundance

Earthworms sampling could be conducted in a total of 488 plots (of an initial target of

500 according to experimental design). The remaining 12 plots were excluded from

the analysis due to difficult field conditions such as rocky areas, piles of wood,

presence of tree stumps, massive presence of roots or spots overlapping with a

forest road. Furthermore, in 7 cases of the 488 plots, the volume of soil needed to be

reduced due to difficult terrain. However, earthworm abundance could still be

calculated since the total volume of the sampled soil was always measured.

In the environmental variable of soil texture, the two types of soil “loamy soil”

and “clay soil” were measured, while no sandy soil were reported from the field.

When investigating which explanatory environmental variables are related to

abundance of earthworm, the final generalized linear mixed-effect model included the

environmental variables that were significant (Table 3). A significance was found for

pH and for the optimum effect of pH (Table 3), indicating the highest earthworm

abundance at around pH of 6 (Figure 9). Soil humidity showed an associated

optimum with earthworm density between a relative humidity of the soil around 70%

(Table 2, Figure 10). An optimum was also found for date (Table 3). Earthworm

abundance increased from April to May and decreased again from mid-May onwards

(Figure 11). The two types of soil texture “loamy soil” and “clay soil” differed

significantly in earthworm abundance (Table 3, Figure 12) with the later representing

the intercept of the model (Table 3). Other variables that showed no significant

relationship were removed from the final model such as temperature, the optimum

effect of temperature, day timing with the two levels: morning and afternoon and

meteo with the two levels: sunny and cloudy.

- 23 -

Table 3: Output of the final generalized linear mixed-effect model comparing environmental variables to earthworm abundance, including the most important explanatory variables. Estimates, Standard errors, t-values and p-values are given for each standardized variables. The intercept refers to soil type: Clay

- 24 -

Figure 9: Predicted earthworm density in relation to pH as obtained from the final mixed-effect model (Table 3). Black points in the background represent raw data of pH; the red line represents the prediction line; dashed blue lines represent 95% credible intervals.

Figure 10: Predicted earthworm density in relation to soil humidity as obtained from the final mixed-effect model (Table 3). Black points in the background represent raw data of soil humidity; the red line represents the prediction line; dashed blue lines represent 95%% credible intervals.

Figure 11: Predicted earthworm density in relation to the season as obtained from the final mixed-effect model (Table 3). Black points in the background represent raw sampling dates; the red line represents the prediction line; dashed blue lines represent 95%% credible intervals.

- 25 -

Figure 12: Predicted earthworm density in relation to the soil texture with the latter characterized by two levels: clay soil and loamy soil (Table 3). No sandy soil was recorded. Black points in the background represent raw data; black bars represent the 95% credible intervals.

3.3 Woodcock presence in relation to earthworm abundance

In this part of the analysis, the aim was to analyze how the presence of the

woodcock was related to the abundance of earthworms. A first overview based on

the boxplot of raw data hints to an obvious difference with higher abundance of

earthworms within home range as compared to absence sites (Figure 13).

Confirmation followed from the generalized linear mixed model showing a strong

positive relationship between abundance of earthworms and the probability of

woodcock presence (binomial mixed effect model controlling for spatial

autocorrelation: (p-value: 2.26E-06; Figure 14). More specifically, areas with

earthworm abundance higher than 0.8 kg/m3 had a probability of woodcocks being

present of 0.75 or above.

For the sections, the boxplot (Figure 15) shows a clear pattern of declining

earthworm abundance from the 30% (most densely used) section of the home

ranges to the 60% and 95% home range sections. Absence plots showed lowest

earthworm abundance. The linear model analysis confirmed significant differences

between the levels (Table 4).

- 26 -

Figure 13: Raw data of earthworm abundance in (Presence) and outside (Absence) of home ranges.

Figure 14: Predicted probability of woodcock presence in relation to earthworm abundance as obtained from the final binomial linear mixed effect model. Black dots show raw data. The blue line represents the prediction from the model and the grey surfaces represent the 95% credible interval.

- 27 -

Table 4: Output of the linear model comparing % of occupancy in the home range in relation to earthworm abundance. Estimates, standard errors, t-values and p-values are given for each variables.

Figure 15: Boxplot show raw data of earthworm abundance in the three home range sections (30%, 60% and 95%) and in the absence sites.

- 28 -

4 DISCUSSION

In this MSc Study, I investigated what food woodcocks find in the Jura mountains and

whether earthworms are a substantial part of woodcock’s food. I than sampled

earthworm abundance in areas where woodcocks were present and compared it with

areas without any recorded presence of woodcock. Earthworm abundance was

highest in humid, slightly acidic, clayey soils and woodcocks clearly preferred areas

with high earthworm abundance. My study gives important insights into types and

availability of woodcock’s food in the Jura mountains which allows to develop

measures for conservation.

Analysis of faeces samples under binocular confirmed substantial presence of

earthworm’s chaetae, highlighting the importance of earthworms as prey item of

woodcocks in the Jura mountains. All the samples each from a different individual

contained earthworm remains. Thus, similar to breeding populations in the U.K.

(Hoodless and Hirons 2007), or wintering birds in France (Granval 1987), the

breeding population of woodcocks in the Jura Mountains can be regarded as an

earthworm specialist. This is hardly surprising and supports the notion that

earthworms are a major food resource of many species of birds (Granval and Aliaga

1988; Duriez et al. 2006). Woodcock metabolism surely needs high intake of energy

for activities such as daily roding of males, parental investment for females and two

migrations a year. To compensate such expense of energy, earthworms seem to be

a convenient food resource for reasons of quantity and quality. Firstly, an average

biomass abundance of 0.44kg/m3 was found on 488 sites visited, suggesting a rather

high availability of earthworm in the Jura Mountains. In comparison, permanent

grasslands of the Swiss Plateau contained between 0.13 and 0.51kg/m3 (Cuendet et

al. 1997), while only 0.006 to 0.021kg/m3 were reported from ploughed fields

(Ducommun 1989). Secondly, earthworms were found to contain a considerable

amount of proteins and lipids (Guerrero 1981), making them a favorable food

resource for high metabolic requirements.

The lack of other soil macrofauna may be explained by the advanced state of

digestion of certain items, meaning that they were not detectable in the fecal

samples. Indeed, in contrast to the earthworm’s chaetae which are easy to identify,

other items might be more degraded and harder to detect. Another reason could be

- 29 -

that very few number of samples were explored. It would have been extremely time

consuming to analyze more samples and search for other preys. The primary aim of

this study was not a detailed analysis of fecal remains but rather confirming the

importance of earthworm as woodcock’s prey and quantifying the availability of this

important prey in the study site throughout the breeding period.

Since earthworms are apparently present in the food of woodcocks in the Jura

Mountains, it was justified to focus on earthworm abundance and their environmental

covariates in the field in detail. Earthworms were present in the majority of visited

sites with 461 sampling squares containing earthworms. They were strictly absent in

only 27 squares and 24 of them were from very acidic soils with pH

- 30 -

However, this was not explored here since the aim was to stay focused on the

breeding season of woodcock.

Importantly, this seasonal dynamics of earthworm abundance is explained by

a number of seasonally changing environmental factors modulating the life cycle

traits (Daniel 1990). For instance, the increase at the beginning of the season

probably reaches a maximum abundance in Mid-May as intra-specific competition for

food increased during development of the juveniles. Scarcity of food was found to

largely slow the different life cycle steps of earthworm owing to intra-specific

competition in L. terrestris (Daniel 1990), and thus affect the dynamics of the

population. However, food availability may differ from one place to another, so any

effects of competition are speculative. The question of the environmental

circumstances that lead to a decrease of earthworm abundance in the second half of

the season remains also unanswered, although a few reasons could be suggested.

For instance, environmental stresses are known to induce earthworm migration to

more favorable environmental circumstances (Pelosi 2006; Daniel 1990). While

predation is known to impact earthworm population density (Daniel 1990; Satchell

1967).

Given the complexity of underlying earthworm dynamics, it seems hard to

predict it for the future. Experimental manipulations would be required if one or

multiple causes should be investigated. There are some models which were created

to predict earthworm density into the future to sustain agriculture (Pelosi 2006). In a

similar way, predicting how earthworm density fluctuates in the Jura Mountains

during the breeding season of woodcocks could certainly reveal some insights on

food resource as limiting factors for woodcocks. Overall, I suggest that the

seasonality needs to be taken into consideration but disentangling its effects remains

difficult.

Whereas predicting earthworm abundance is out of scope in this study, I found

some external abiotic factors that proofed to be important for earthworm abundance.

For instance, soil humidity showed a strong positive correlation with the abundance

of earthworms. This is hardly surprising since soil humidity is fundamental for the

physiology of earthworm (Curry 1998; Satchell 1967). Indeed, respiration of

earthworms is exchanged through some specialized cells on the skin that needs to

stay constantly moist to enable the permeability of gases (Curry 1998). Hence, they

need an environment with a certain humidity to prevent that the body dries.

- 31 -

Earthworms in the Jura Mountain showed a tolerance range for soil humidity between

30% and 85%, whereas soil humidity of 60% was optimal. Similarly, earthworms

tolerated a pH range from pH 4.5 to 7 with an optimum around pH 6. Although I only

found very few areas with very acidic soils, this results confirms previous findings that

earthworms tend to favor more neutral soils (Curry 1998, Satchell 1967).

Moreover, a significance was found for the soil texture and the earthworm

abundance. This study confirmed that earthworms showed a preference for clay and

loamy soils similar to what Nordström and Rundgren (1974) found, although I could

only proceed to a qualitative analysis of soil texture. Importantly, the soil texture has

an influence on soil hydraulic properties (Gobat et al. 2003). The grain size

distribution controls the quantity of air and water that a soil can hold. More

specifically, the difference of rate of sand, loam or clay that a soil contains determine

the amount of water entering and moving through the soil. A higher rate of loams and

clays than sands are known to enable the soil to contain considerable moisture

(Gobat et al. 2003; Nordström and Rundgren 1974). Hence, Jura soil probably stays

sufficiently humid for earthworms as it contains a certain amount of clays and loams.

While sandy soils were not found during this fieldwork.

Surprisingly, temperature did not show any significant relationship to

earthworm abundance, although temperature is known to be fundamental in

determining earthworm activity (Satchell 1967). There was no relationship even

though measurements of temperature were performed 10 times a day from morning

to late afternoon. Air temperature ranged from 5.5°C to 26.5°C throughout the

season while the greatest difference of air temperature from morning to afternoon in

a single day was 6.5°C. Air temperature varied during the whole season and between

morning and afternoon of the same day, but variation in soil temperature was

probably less pronounced. The soil likely acted as a thermal buffer reducing the

variation in soil temperature in the Jura Mountains. Hence, I suggest for next studies

to measure soil temperature instead of air temperature to control how soil

temperature varies, and if this variation is related to earthworm abundance.

Prior to the start of the field work, the question of timing of earthworm

sampling was repeatedly discussed since earthworms are known to show daily

migratory patterns (Lee 1985). Thus, I recorded for each sample whether it was

taken in the morning or in the afternoon. Afternoon samples seemingly revealed

slightly more earthworms than in the morning, but this differences were not

- 32 -

significant. Indeed, an average of abundance of 0.46kg/m3 was measured in the

afternoons and 0.41kg/m3 during the mornings. To investigate daily dynamics of

earthworm abundance in more detail, I suggest to spread sampling more thoroughly

throughout the day and also into night time. Duriez et al. (2006) demonstrated the

efficiency and relevance of nocturnal sampling earthworms, as it takes into

consideration both the greater nocturnal activity of worms at night and nocturnal

foraging activity of wintering woodcocks (average of 0.75 kg/m3 in meadows). Hence,

a higher density of worms was probably expected if sampling would have been

performed at night. However, as previously mentioned, my study concerned breeding

birds and activity changes between breeding and wintering periods. Importantly, if

woodcocks forage during daytime in the Jura Mountains, diurnal worm availability

might respond to the food requirements of woodcocks. And the availability I found is

obviously sufficient to maintain presence of woodcock in the area.

Finally, there was no significant relationship of the meteo and earthworm

abundance. Cloudy and sunny measurements did not significantly differ in the

abundance found. During periods of cloudy days, rain was not necessarily falling.

Thus, the difference of effect between sunny and cloudy was probably less strong on

earthworm’s activity and probably depends on rain that falls. This coincide with the

fact that no sampling was performed during rainy days, although strong rain can

cause emergence of earthworm near the surface (Pelosi 2008). Hence, a stronger

relationship would probably be found if sampling was performed under rain.

Importantly, this reveal the possibility of co-varying environmental factors

because meteo showed correlations with soil humidity and air temperature. Although

their effects are hardly disentangled from each other, the fact of adding them all to

one model made the strongest effect of soil humidity significant, whereas correlated

and less important effects such as air temperature and meteo did probably not. This

can be reasons for such unexpected non-significance. The reason why humidity had

the strongest effect is probably because it was the effect measured with the highest

precision. Similarly, since soil humidity was highly significant and showed strong

correlation with temperature, it could be that air temperature is not important as long

as soils stay humid.

Overall, there is a diversity of soils and conditions in the Jura mountains

providing space earthworms in changing abundance. The population is

heterogeneously distributed in relation to some abiotic factors. Important factors such

- 33 -

as pH, soil humidity and soil texture are important and allow predicting earthworm

abundance in the Jura Mountains. On the other hand, there was a strong seasonal

dynamic which I cannot fully explain.

Another central question of my study was whether woodcocks preferred areas with

high earthworm abundance. Indeed, my analysis showed such a positive relationship

in 2 levels: Firstly, the presence of woodcocks was more likely in forests where

earthworm abundance was high and earthworm abundance was lower at the

absence sites. Secondly, earthworm abundance increased from the periphery of the

home range, to the central and to the most intensively used core, suggesting that

woodcocks actively search for sections of high earthworm abundance within their

home range. These correlative results represent the most important outcome of this

study since it strongly indicates that food availability is an important driver

determining woodcock’s habitat selection on breeding grounds. At least, this is the

case for males of woodcocks. It supports the results found on wintering birds

showing preference for meadow habitat with the highest earthworm biomass (Duriez

et al 2005), and confirms that woodcocks actively search and select places with high

amount of earthworms all-year round.

Interestingly, this is apparently the case even if woodcock’s feeding strategy

importantly changes between breeding time and winter. (Brüngger and Estoppey

2008, Del Hoyo et al. 1996). This lead to a central question of why woodcocks do not

feed all-year round in meadows (habitat with highest earthworm availability), knowing

that food is a major habitat characteristic. Indeed, the lower average of earthworm

abundance I found in the forest compared to what Duriez et al. (2006) found in

meadows (0.44kg/m3 in forest vs. 0.75kg/m3 in meadows) support this question.

Whereas it is also known that the Jura Mountains contains meadow soils that attracts

feeding woodcocks in autumn at night (Rocheteau et al. 2015). The reasons of this

change in lifestyle are still poorly discussed. It is likely that woodcocks readjust

feeding strategy not exclusively for the highest earthworm availability, but seemingly

adapt their search for earthworm hotspots according to other external factors. For

instance, during crucial time of reproduction in spring, the nocturnal habitat with the

highest earthworm abundance is probably not sufficient to attract woodcocks since

investing time in reproduction become more important. Whereas, crepuscular and

predawn displaying activities probably do not give enough time to feed at night and

thus constrain woodcocks to forage at daytime. But as reproduction activity still

- 34 -

demands considerable energy, woodcocks still actively search for earthworm

hotspots at daytime. Interchange diurnal or nocturnal foraging strategy may represent

a compromise between reproduction investment and food availability. In the other

hand, diurnal habitat with the highest earthworm abundance is probably not sufficient

to convince woodcocks if there is no cover to protect them against predators

(Hoodless and Hirons 2007; Duriez et al. 2005; Hirons and Johnson 1987). This

could explain why they seems prefer to stay foraging in dense forest during breeding

time rather than going out in meadows. In contrast, out of the breeding season,

nights probably allow to feed inconspicuously in more open areas (in meadows) with

the highest food abundance. Shifting by feeding in either forest habitat or in

meadows represent another trade-off between food availability and predation risks as

suggested before. Hence, while I confirmed the importance of food availability, I

suggest to consider the possibility that it is not an exclusive factor driving habitat

selection of woodcocks and look at whether it is more likely associated with other

factors such as protection against predators and reproduction investment.

Although woodcocks regularly change their lifestyle for such speculative

reasons, it must be overall underlined that woodcocks are clearly selecting and

favoring areas with high availability of their main food all year-round. In other words,

earthworms are as important on breeding grounds as they are during winter. It seems

now clear that earthworms have a major importance in the habitat selection of

woodcocks and therefore reopens the debate regarding to the controversial topic of

food as a mechanism driving habitat use in birds.

Finally, this result can also open discussions regarding woodcock’s decline in

Switzerland. Scarcity of earthworms as a factor causing the decline could be

adequately envisaged. Since high earthworm abundance is favored by woodcocks, it

can be easily assumed that unavailable earthworm may have negative effects on the

population. This study is not sufficient to figure out direct causality between

woodcock’s decline and earthworm availability, but the correlative outcomes can be

seriously used as a predictor.

- 35 -

5 CONCLUSION

In summary, the study was conducted in three steps. Firstly, a qualitative analysis

allowed to detect expected bristles and confirmed that earthworms are part of the

food of woodcocks in the Jura Mountains. Although this step did not allow to define

the exact diet of the woodcock, it confirmed for the first time that earthworms depict

an important prey of the woodcock in Switzerland.

The second part of the study clarified which of the important environmental

variables might drive earthworm abundance. The seasonal dynamic of abundance

was suspected to arise due to some fundamental but unknown external factors

impacting life cycle traits of earthworms. Determining such environmental factors was

out of scope in this study as experimental models are needed. But this, in a next

step, could predict how woodcocks can be exposed to food limitation throughout its

breeding season. Furthermore, soil humidity, pH, and soil texture (with two levels:

clay and loamy soil) were correlated to the heterogeneous abundance of earthworm.

Earthworms show characteristic tolerance ranges in respect to these soil variables

which apparently is important for woodcock’s distribution.

Since the woodcock is regarded as an earthworm specialist, the last part of the

study mainly aimed at the question: do woodcocks actively search sites of high

earthworm abundance? Indeed, I found a strong relationship of earthworm

abundance with sites where woodcocks spent most of their time. In other words, sites

with high abundance of earthworms were more likely to harbor woodcocks. Indeed,

as it is often the case in ecological studies, I can only show a correlative relationship

between earthworms and woodcocks. It seems unrealistic to experimentally

manipulate food abundance to see whether this causally affects woodcocks. On the

other hand, my results whereas a graduation of few, little and high earthworm

abundance in the different sections is a very strong indication of causal relationship.

Hence, this study reveals the possibility of seriously considering earthworm

abundance as one of the important factor driving habitat selection by woodcock in the

Jura Mountains. Finally, the study provides additional tools of what to consider in the

conservation measures to ensure the persistence of the species in Switzerland in the

future.

- 36 -

Conservation perspectives

Prior to any conservation actions, determining responsible factors causing the

decline of a species is crucial but challenging. The question whether such decline is

due to a single factor, multiple factors or due to the interaction of factors surely

requires intensive investigations. In the case of the woodcock, more work is needed

to determine the exact factors affecting the population. There are still several

uncertain parameters to clarify and fundamental understanding of the species in

Switzerland is lacking. As suggested before (Mollet 2015), other thematic such as the

development of forest structure, (human) disturbance during the breeding time,

hunting pressure or increase of natural predation have to be investigated as quickly

as possible to implement right conservation measures and ensuring the long-term

persistence of breeding Eurasian Woodcock throughout Switzerland. With such a

secretive behaviour and a specialist’s lifestyle, forest structure in the Jura Mountains

certainly play an important role during breeding time. I suggest therefore to invest

more work to understand the relationship between Eurasian Woodcocks, plant

communities (habitat/protection) and earthworms (food) in order to initiate and

develop some optimal conservation properties.

Nonetheless, results of this study reveal a predominant relation between woodcock’s

population and the availability of its main food. It also reveals the possibility of

predicting woodcock presence by mapping earthworm hotspots. We now know that

these important areas must include certain favorable soil physical conditions I found

to enable earthworm presence. I also suggest to control the abundance of

earthworms in region where woodcock is reported extinct. This could reveal insights

of unavailable food abundance as a cause of population decline. If scarcity of

earthworm population is found to cause major decline of woodcock population,

efficient modelling of population dynamics of earthworms has to be investigated. This

may allow to determine what prevent earthworm communities to sustain in high

proportion. Then initiate actions to maintain a certain density of earthworm would

probably allow the woodcock to have again access to sufficient abundance of its

prey. This, of course, goes along with measures such as protection of humid forest

- 37 -

soils by reducing drainage or intensive harvest of wood and increase number of

protected areas throughout its range.

Acknowledgements

First of all, I wish to express a huge thank to Dr. Benjamin Homberger for having

been my main supervisor during the entire study, but above all, for sharing his

extensive knowledge, for his relentless assistance in many ways, for his valuable

help in statistics, to have encourage me through difficult moments, to have followed

me in the field, and for his friendship.

I would also like to thank Dr. Martin Grüebler, my other main supervisor, for giving

me this great opportunity to do this master thesis and allowing me to be part to this

exciting woodcock project and for sharing with me numerous ideas.

I am also grateful to the Swiss Ornithological Institute for having funded my expenses

during the work, for covering my travel and borrowing equipment. Without this the

study would not have been possible. Also, I wish to thank Yves Gonseth who is the

project leader of this national project.

Importantly, I wish to thank Christophe Praz, my official Neuchâtel University

supervisor, for having showed the enthusiasm to follow my work and for his helpful

advice.

I will never forget and feel very thankful to Claire-Le Bayon for her precious advice,

and for sharing her extensive knowledge on earthworms and how to conduct my

analysis on earthworm’s faeces.

I am grateful to my fieldwork team from Vogelwarte Sempach and CSCF: Marine

Delmas, Vincent Rocheteau, Nicolas Vial and Charlotte Warburten for helping me in

the field and sharing great moments during my time in Fleurier NE.

Finally, I want to mention all other people who shared ideas with me or gave advices

or simply encouraged me during this year. Thanks to Laura Chappuis, Céline Bell,

- 38 -

Lionel Maumary, Alida Kropf, François Estoppey, Edward Mitchell, Neil Villard, to my

close friends and of course, to my father and my mother.

Reference Andris, K., Westermann, K. (2002). Brutverbreitung, Brutbestand und Aktionsraum-Grösse der Waldschnepfe (Scolopax rusticola) in der südbadischen Oberrheinebene. Naturschutz südl. Oberrhein 3: 113–128. Aradis, A., Landucci, G., Tagliavia, M., Bultrini, M. (2015). Sex Determination of Eurasian Woodcock Scolopax rusticola: a molecular and morphological approach. Avocetta. 39. Bachelier, G. (1978). La faune des sols, son écologie et son action, IDT N°38. ORSTOM, Paris, 391 pp. Bhatti, H. K. (1962). Experimental study of burrowing activities of earthworms. Agri. Pakistan. 13, 779-794. BirdLife International (2016). Scolopax rusticola. The IUCN Red List of Threatened Species 2016. Blouin, M., Hodson, M. E., Delgado E., A., Baker, G., Brussaard, L., Butt, K.R., Dai, J., et al. (2013) A review of earthworm impact on soil function and ecosystem services. Eur. J Soil Sci. 64:161–182 Bouché, M. B. (1972). Lombriciens de France: Ecologie et Systématique. INRA Ann. Zool. Ecol. Anim. Publication, France, 671 pp. Bouché, M.B., Aliaga, R. (1986). Contre une dégradation physique et chimique des sols et pour leur optimisation économique, l’échantillonnage des lombriciens: une urgente nécessité. La défense des végétaux 242, 30–36. Bouché, M.B., Gardner, R.H. (1984). Earthworms functions VIII – population estimation techniques. Revue d’Ecologie et de Biologie du Sol 21, 37–63. Braña, F., Gonzalez-Quiros, P., Prieto, L., González, F. (2013). Spatial Distribution and Scale-Dependent Habitat Selection by Eurasian Woodcocks Scolopax rusticola at the South-Western Limit of its Continental Breeding Range in Northern Spain. Acta Ornithologica. 48. 27-37. Brüngger, M., Estoppey, F. (2008). Exigences écolgiques de la bécasse des bois Scolopax rusticola dans les Préalpes de Suisse Occidental. Burt, W.H. (1943). Territoriality and Home Range Concepts as Applied to Mammals. Journal of Mammalogy, 24 [3], pp. 346. DOI: 10.2307/1374834. Calenge, C. (2006). The package adehabitat for the R software. Ecological Modelling [197], pp. 516–519.

- 39 -

Carlisle, J. D., Holberton, R. L. (2006). Relative efficiency of fecal versus regurgitated samples for assessing diet and the deleterious effects of a tartar emetic on migratory birds. Journal of Field Ornithology, 77: 126-135. Cuendet, G., Suter, E., Stähli, R. (1997). Peuplement lombriciens des prairies permanents du Plateau suisse. Cahier Environn. 291, Sol. OFEFP, Berne Daniel, O. (1990). Life cycle and population dynamics of the earthworm Lumbricus terrestris L. /. Del Hoyo, J., Elliott, A., and Sargatal, J. (1996). Handbook of the Birds of the World, vol. 3: Hoatzin to Auks. Lynx Edicions, Barcelona, Spain. Ducommun, A. (1989). Influence des boues d’épuration et du fumier sur les mincroinvértébrés édaphiques de quelques cultures intensives du Grand-Marais (Plateau Suisse). Thèse de doctorat, Univéristé de Neuchâtel. Duffy D. C., Jackson, S. (1986). Diet sutdies of Seabirds : a review of methods. Col. Waterbirds 9 :1-17. Duriez, O., Ferrand, Y., Binet, F., Corda, E., Gossmann, F., Fritz, H., (2005). Habitat selection of the Eurasian woodcock in winter in relation to earthworms availability. Biological Conservation. 122. 479-490. Duriez, O., Ferrand, Y., Binet, F. (2006). An Adapted Method for Sampling Earthworms at Night in Wildlife Studies. Journal of Wildlife Management. 70. 852-858. 10.2193/0022-541X(2006)70[852:AAMFSE]2.0.CO;2. Edwards, C. A. (1983). Earthworm ecology in cultivated soils. Pages 1 2S137 in J. E. Satchell, editor. Earthworm ecology, from Darwin to vermiculture. Chapman & Hall, London, United Kingdom.

Edwards, C. A., Bohlen, P. J. (1996). Biology and Ecoloy of Earthworms 3rd ed. Chapman and Hall, London, 426 pp. Eichinger, E., Bruckner, A., Stemmer, M. (2007). Earthworm expulsion by formalin has severe and lasting side effects on soil biota and plants. Ecotoxicol Environ Saf 67:260–266 Estoppey, F. (2001a). Le déclin de la population de Bécasse des bois (Scolopax rusticola) du Jorat (Vaud, Suisse). Nos Oiseaux, 48: 83-92 Estoppey, F. (2001b). Suivi démographique des populations nicheuses de bécasse des bois Scolopax rusticola en Suisse occidentale de 1989 à 2000. Nos Oiseaux, 48 (2) : 105-112. Fadat, C. (1995). La Bécasse des bois en hiver. Ecologie, Chasse, Gestion. Maury presse, Clermont-l’Hérault, France.

- 40 -

Ferrand, Y., Gossmann, F. (2009). La bécasse des bois. Histoire naturelle. Ed. Effet de lisière: 222 pages. Ferrand Y. (1993). A census method for roding Eurasian Woodcocks in France. In: Longcore J. R., Sepik G. F. (eds). Proceedings of the Eighth American Woodcock Symposium. U.S. Fish and Wildlife Service Biological Report 16: 19–25. Ferrand Y., Gossmann F. (2000). Trend in the breeding Woodcock population in France from 1992 to 1997. In: Kalchreuter H. (ed.). Proceedings of the Fifth European Woodcock and Snipe Workshop, Czempin, Poland. Global Series 4, International Wader Studies 11: 34–36. Ferrand Y., Gossmann F., Bastat, C., Guénézan, M. (2008). Monitoring of the wintering and breeding Woodcock pop- ulations in France. Revista Catalana d’Ornitologia 24: 44–52. Ferrand Y., Landry, P. (1986). Répartition spatiotemporelle des bécasses des bois, Scolopax rusticola, à la croule en Forêt Domaniale de Rambouillet (Yvelines). Gibier Faune Sauvage 3: 115–141. Fisher, M. (1905). The toxic effect of formaldehyde and formalin. Pathological laboratory of rush medical college, Chicago. Fragoso C., Lavelle, P. (1992). Earthworm communities in tropical rain forests. Soil Biology and Biochemistry, 24: 1397–1409. Gelman, A., Hill, J. (2006). Data Analysis Using Regression and Multilevel/Hierarchical Models. Cambridge University Press. Gonseth, Y., Bohnenstengel, T. (2015). Projet Bécasse des Bois : Rapport de la phase préparatoire (juin 2014 à avril 2015). Rapport 10 pp. Gobat, J. M., Aragno, M., Matthey, W. (2003). Le sol vivant. Bases de pédologie, biologie des sols. (2 ed.). Lausanne: Presses Polytechniques et universitaires romandes. Granval, P. (1987). Régime alimentaire diurne de la Bécasse des bois (Scolopax rusticola) en hivernage: approche quantitative. Gibier Faune Sauvage 4, 125–147. Granval, P. (1988). Approche écologique de la gestion de l’espace rural: des besoins de la Bécasse (Scolopax rusticola L.) à la qualité des milieux. Thèse de doctorat, Université de Rennes I, Rennes, France. Granval, P., Aliaga, R. (1988). Analyse critique des connaissances sur les prédateurs de lombriciens. Gibier Faune Sauvage 5, 71–94. Granval, P., Muys, B. (1992). Management of forest soils and earthworms to improve woodcock (Scolopax sp.) habitats : a literature survey. Gibier Faune Sauvage 9, 243–256.

- 41 -

Granval, P., Bouché, M.B. (1993). Importance of meadows for wintering Eurasian woodcock in the west of France. In: Longcore, J.R., Sepik, G.F. (Eds.), Eighth American Woodcock Symposium, vol. 16. US Fish and Wildlife Service, Biological Report 16, p. 135 Guerrero, R.D. (1981). The culture and use of Perionyx excavatus as a protein resource in the Phillippines. Dorwin Centenary Symp. On Earthworm ecology (pp 250). Inst. Terrestrial Ecology UK. Gunn, A. (1992). The use of mustard to estimate earthworm populations. Pedobiologia 36:65–67 Hartley, P.H.T. (1948). The assessment of the food of birds Ibis 90: 361-38. Hausen, H. Hydrobiologia (2005). Chaetae and chaetogenesis in polychaetes (Annelida) 535: 37. https://doi.org/10.1007/s10750-004-1836-8 Hirons, G., Bickford-Smith, P.B. (1983). The diet and behaviour of Eurasian Woodcock wintering in Cornwall. In proceeding of the 2nd European Woodcock and Snipe Workshop. Fordingbridge, England, 30 March-1st April 1982 : 11-17. Hirons, G., Johnson, T. H. (1987). A quantitative analysis of habitat preferences of Woodcock Scolopax rusticola in the breeding season. Ibis 129: 371–381.

Hirons, G. (1978). Winter food of woodcock in Britain. Newsletter, 4, 3-4 Hirons, G. (1988). Habitat use by woodcock during the breeding season. In. Acts of the third European Woodcock and snipe workshop. ONC, Paris, 42-47 Hoodless, A. N., Hirons, G. (2007). Habitat selection and foraging behaviour of breeding Eurasian Woodcock Scolopax rusticola : A comparison between contratsting landscapes. Ibis 149 (Suppl.2) : 234-249 Hounsome, T., O’Mahony, D., Delahay, R. (2004). The diet of Little Owls Athene noctua in Gloucestershire, England. Bird Study, 51: 282–284. IARC. (1995). IARC monographs on the evaluation of carcinogenic risk of chemicals to humans: Wood dusts and formaldehyde. Vol. 62. World Health Organzation, Lyon, France, 37: 500. DOI: 10.1007/BF02908826 Jones, C.G., Lawton, J.H., Shachak, M. (1994). Organisms as ecosys- tem engineers. Oikos 69:373–386 Knaus, P., Antoniazza, S., Wechsler, S., Guélat, J., Kéry, M., Strebel, N., Sattler, T. (2018). Atlas des oiseaux nicheurs de Suisse 2013-2016. Distribution et évolution des effectifs des oiseaux en Suisse et au Liechtenstein. Station ornithologique suisse, Sempach. Kouba, M., Bartos, L., Tomasek, V., Popelkova, A., Stastny, K., Zarybnicka, M. (2017). Home range size of Tengmalm’s owl during breeding in Central Europe is determined by prey abundance. PLoS ONE 12(5): e0177314.

- 42 -

Lauer, E., Sibut, P., Dutertre, B., Colinon, S., Ferrand, Y., Duchamp, C. (2006). Identification test of suitable Woodcock breeding habitats in mountain areas. S. 66–70 in: Y. Ferrand: Sixth European Woodcock and Snipe Workshop - Proceedings of an International Symposium of the Wetlands International Woodcock and Snipe Specialist Group, 25-27 November 2003, Nantes, France. Wetlands International, Wageningen, Netherlands. Lanz, M. (2008). Lebensraumpotenzial und Habitatnutzung der Waldschnepfe in den nordöstlichen Voralpen. Diplomarbeit, Zürcher Hochschule für angewandte Wissenschaften. Lavelle, P. Spain, A.V. (2001). Soil Ecology. Kluwer Scientific, Amsterdam. Lee, K.E., (1985). Earthworms. Their ecology and relationships with soils and land use. Academic Press Australia, Sydney, Australia. Lutz, M., Jensen, F.P. (2005). European Union management plan for Woodcock Scolopax rusticola 2006–09. European Union, Strasbourg. Maumary, L., Duperrex, H., Cloutier, J., Vallotton, L. (2013). Première nidification du Circaète Jean-le-Blanc Circaetus gallicus en Suisse. Nos oiseaux. 60. 3-24. Maumary, L., L. Vallotton, P. Knaus. (2007). Les oiseaux de Suisse. Station ornithologique suisse, Sempach, et Nos Oiseaux, Montmollin Matthey, W., Zettel, J., Bieri, M. (1990). Invértébrés bioindicateurs de la qualité des sols agricoles/Wirbellose Bodentiere als Bioindikatoren für die Qualität von Landwirtschaftsböden. Programme national de recherche 22: SOL, Liebefeld-Bern Mollet, P. (2015). La bécasse des bois (Scolopax rusticola) en Suisse – Synthèse 2014. Station ornithologique Suisse, Sempach. Mulhauser, B., Zimmermann, J.-L. (2010a). Fidélité des mâles de Bécasse des bois Scolopax rusticola à leur site de reproduction. Alauda 78 (1) : 27-39 Mulhauser, B., Zimmermann, J.-L. (2010b). Individuelle Erkennung und Bestandserfas- sung bei der Waldschnepfe Scolopax rusticola anhand von Gesangsmerkmalen balzender Männchen. Ornithol. Beob., 107 : 39-50 Mulhauser, B., Zimmermann, J.-L. (2015). Suivi démographique de la Bécasse des Bois Scolopax rusticola en période de reproduction dans le canton de neuchâtel (Suisse) entre 2001 et 2010. Mulhauser, B. (2001). Situation de la Bécasse des bois Scolopax rusticola en période de reproduction dans le canton de Neuchâtel (Suisse) entre 1998 et 2000. Nos Oiseaux 48: 93–104.

- 43 -

Mulhauser, B. (2002). Suivi spatio-temporel des aires de croule des bécasses des bois Scolopax rusticola à l'aide de recensements simultanés. Alauda 70: 121–130. Muys B., Granval, P. (1997). Earthworms as bio-indicators of forest site quality. Journal of Soil Biology and Biochem- istry, 29: 323–328. Nordström, S., Rundgren, S., (1974). Environmental factors and lumbricid associations in southerns Sweden. Pedobiol. 14, 1-27. Oehm, J., Thalinger, B., Eisenkölbl, S., Traugott, M. (2017). Diet analysis in piscivorous birds: What can the addition of molecular tools offer?. Ecology and Evolution. 7. 10.1002/ece3.2790. Paris, P. (1914). Examen du contenu stomacal de quelque rapaces. RFO, LXIV-LXV 357- 359.

Pelosi, P. (2008). Modélisation de la dynamique d’une population de vers de terre

Lumbricus terrestris au champ. Contribution à l’étude de l’impact des systèmes de

culture sur les communautés lombriciennes. Sciences de la Terre. AgroParisTech,

Français.

Poier, K.R., Richter, J., (1992). Spatial distribution of earthworms and soil properties in an arable loess soil. Soil Biology and Biochemistry 24, 1601–1608. Pienkowski, M.W., Fems, P.N., Davidson, N.C., Worrall, D.H., (1984). Balancing the budget: measuring the energy intake and requirements of shorebirds in the field. In: Evans P.R., J.D. Goss-Custard & W.G. Hale (eds) Coastal waders and wildfowl in winter: 29-56. Cambridge University Press, Cambridge. Rocheteau, V., Gremaud, J., Rime, Y., Gonseth, Y., Bohnenstengel, T. (2015). Projet Bécasse des Bois : Rapport des tests méthodologiques (juin à août 2015). Rapport 45pp. Rosenberg, K.V., Cooper, R.J. (1990) : Approaches to avian diet analysis. Studies in Avian Biology 13: 80-90. R Core Team. (2016). R: A language and environment for statistical computing. URL https://www.r-project.org/ [accessed 6 February 2018] Rossi, J.P., Lavelle, P., Albrecht, A., (1997). Relationships between spatial pattern of the endogeic earthworm Polypheretima elongata and soil heterogeneity. Soil Biology and Biochemistry 29, 485– 488. Salehi. A., Ghorbanzadeh. N., Kahneh. E. (2013) Earthworm biomass and abundance, soil chemical and physical properties under different poplar plantations in the north of Iran. JOURNAL OF FOREST SCIENCE, 59, 2013 (6): 223–229 Satchell, J. E., (1967). Lumbricidae. In: Burges, A. et Raw, F. (eds), Soil Biology. Academic Press, London, pp. 259-322.

- 44 -

Satchell, J. E., (1969). Methods of sampling earthworm populations. Pedobiol. 9, 20-25. Satchell J. E., (1971). Earthworms. In: Philipson J (ed) Methods of study in quantitative soil ecology: population. Production and energy flow. Blackwell Scientific Publications, Oxford, pp 107–127 Schmid, H., Luder, R., Naef-Daenzer, B., Graf, R., Zbinden, N. (1998). Atlas des oiseaux nicheurs de Suisse. Distribution des oiseaux nicheurs en Suisse et au Lichtenstein en 1993-1996. Station ornithologique Suisse. Sempach. Steinfatt, O. (1938). Das Brutleben der Waldschnepfe. J. Orn., 86 :379-424 Tester, J. R., Watson, A. (1973). Spacing and territoriality of woodcock Scolopax rusticola based on roding behaviour. Ibis 115: 135–138. Van Winkle, W. (1975). Comparison of several probabilistic home range models. Journal of Wildlife Management 39:118–123. Whiterby, H.F., Jourdain, F.C.R., Ticehurst, C.B., Tucker, B.W. (1940). The handbook of British Birds. Vol. 4 184.192 Worton, B. J. (1989). Kernel methods for estimating the utilization distribution in home range studies. Ecology 70:164–168. Wroot, A. (1985). A Quantitative Method for Estimating the Amount of Earthworm (Lumbricus terrestris) in Animal Diets. Oikos, 44(2), 239-242.