Impact of Formica exsecta Nyl. on seed bank and vegetation patterns in a subalpine grassland...

Impact of Formica exsecta Nyl. on seed bank and vegetationpatterns in a subalpine grassland ecosystemM. Schutz1, C. Kretz1, L. Dekoninck1,2, M. Iravani1 & A. C. Risch1

1 Swiss Federal Institute of Forest, Snow and Landscape Research, Birmensdorf, Switzerland

2 Department of Environmental Sciences, Wageningen University, Wageningen, The Netherlands

Introduction

Seed dispersal is crucial for the life cycle of vascular

plants and plays an important role in plant commu-

nity functions such as seed bank formation, seedling

recruitment, vegetation composition and succession

or plant species diversity (Nathan and Muller-Lan-

dau 2000; Fenner and Thompson 2005; Forget et al.

2005). Seed dispersal may, for example, prevent

competition among seedlings, or between seedlings

and the parent plants, may enable plant encroach-

ment into unoccupied sites, or favour establishment

of new genotypes in a changing environment (e.g.

Kozlowski 1972). Consequently, seeds of many

plants are adapted to dispersal by long distance vec-

tors, of which wind and animals have been reported

to be the most important ones (e.g. Grime et al.

1988; Bazzaz 1996; Tackenberg et al. 2003). In par-

ticular, seed dispersal by animals (zoochory) has

been found to be important for grassland vegetation

dynamics (e.g. Welch 1985; Kelrick et al. 1986; Malo

and Suarez 1995a; Pakeman et al. 1999; Bakker and

Olff 2003) and shows many different adapta-

tions ranging from active or passive internal

Keywords

ant mounds, European alps, myrmecochory,

seed dispersal, subalpine pastures

Correspondence

Martin Schutz (corresponding author), Swiss

Federal Intstitute of Forest, Snow and

Landscape Research, CH-8903 Birmensdorf,

Switzerland. E-mail: [email protected]

Received: June 18, 2007; accepted: March 8,

2008.

doi: 10.1111/j.1439-0418.2008.01293.x

Abstract

The mound building ant Formica exsecta Nyl. is widely distributed in

grassland ecosystems of the Central European Alps. We studied the

impact of these ants on seed bank and vegetation patterns in a 11 ha

subalpine grassland, where we counted over 700 active ant mounds.

The mounds showed a distinct spatial distribution with most of them

being located in tall-grass, which was rarely visited by ungulates (red

deer; Cervus elaphus L.). Heavily grazed short-grass, in contrast, seemed

to be completely avoided by ants as only few mounds were found in

this vegetation type. The species composition of the ant mound and

grassland seed banks was quite similar, i.e. from 15 common plant spe-

cies 12 were found in both seed bank types. We found the same propor-

tions of myrmecochorous seeds in ant mound and grassland soil

samples. In contrast, the number of seeds was 15 times higher in mound

compared with the grassland soil samples. Also, the vegetation growing

on ant mounds significantly differed from the vegetation outside the

mounds: graminoids dominated on ant mounds, herbaceous and myr-

mecochorous species in the grassland vegetation. We found significant

continuous changes in vegetation composition on gradients from the ant

mound centre to 1 m away from the mound edge. Overall, F. exsecta

was found to have a considerable impact on seed bank and vegetation

patterns in the grassland ecosystem studied. These insects not only

altered grassland characteristics in the close surrounding of their

mounds, but also seem to affect the entire ecosystem including, for

example, the spatial use of the grassland by red deer.

J. Appl. Entomol.

J. Appl. Entomol. 132 (2008) 295–305 ª 2008 The AuthorsJournal compilation ª 2008 Blackwell Verlag, Berlin 295

(endozoochory) to external (epizoochory) dispersal.

Zoochory is mainly found in three animal groups:

mammalian herbivores, birds (Malo and Suarez

1995b; Pakeman et al. 2002; Myers et al. 2004;

Mouissie et al. 2005) and ants (Sernander 1906; Ulb-

rich 1939; Muller-Schneider 1977, 1986; Beattie

1985; Grime et al. 1988).

In our study, we will focus on seed dispersal by

ants as they are dominant components of most

invertebrate communities (Holldobler and Wilson

1990), but little is known about the general ecologi-

cal consequences that seed dispersal by these insects

has. Even though many studies have been con-

ducted on the dispersal of seeds through ants (e.g.

Sernander 1906; King 1976; Abramsky 1983; Van

Tooren 1988; Gorb et al. 2000; Gorb and Gorb 2003,

Dostal 2005; Dauber et al. 2006) it is hardly to

derive from those how ants affect ecosystem pro-

cesses such as seed bank formation or vegetation

dynamics. The reason for this is that the selection of

seeds varies from ant species to ant species, and

strongly depends on the vegetation type and the

abundance of seeds with particular characteristics

such as elaiosomes (=myrmecochorous plant spe-

cies). Consequently, dependent on the ant species

and ecosystem type under study, preferences for

large (Abramsky 1983; Mittelbach and Gross 1984)

as well as small seeds have been reported (Davidson

and Morton 1981). Some studies stated that seeds

with elaiosomes may be preferred by ants or that e-

laiosome size matters for the insects (Hughes and

Westoby 1992; Mark and Olesen 1996), while others

found that seeds without these lipid-rich additions

were collected (Gorb et al. 1997; Retana et al. 2004).

It also remains unclear where the collected seeds are

stored as it has been reported that the ants keep

them in the mounds (Davidson and Morton 1981;

Oostermeijer 1989), discarded them on piles outside

of the mounds (Beattie 1985; Dostal 2005), or at the

borders of the territory (Gorb and Gorb 2003).

Despite of being important for seed dispersal mound

building ants also create open sites of low vegetation

cover. These ‘low cover’ sites are thought to favour

both seed germination and seedling establishment,

and therefore indirectly affect vegetation patterns.

Seeds deposited in ant mounds may benefit from pro-

tection against predators (Turnbull and Culver 1983;

Gibson 1993) and seedlings grow better on ant

mounds because of reduced competition with other

plants (Handel 1978; Oostermeijer 1989, Dean et al.

1997) and increased soil fertility (Folgarait 1998).

Ant–plant interactions can considerably and differ-

ently alter vegetation dynamics depending on the

ecosystem under study. Ecosystems in the European

Alps currently are undergoing considerable land use

changes as agricultural practices are becoming eco-

nomically less viable (Bantzing 1996; Tasser et al.

2007). As a consequence, the vegetation develop-

ment within these ecosystems will be driven by

other factors than management in the near future.

Ants, in particular the ones that build aboveground

organic mounds, prefer areas with low disturbance

(King 1981; Andersen and Sparling 1997; Beever

and Herrick 2006), therefore it is likely that the

activity of these insects will become more important

in abandoned ecosystems of the European Alps. The

overall objectives of our study were to assess ant–

plant interactions in a subalpine grassland ecosystem

in the Central European Alps that was abandoned

almost 100 years ago, and where nests of the mound

building ant Formica exsecta Nyl. (narrow-headed ant)

are found in high density. More specifically, we esti-

mated the impact of this ant species on seed bank

and vegetation patterns by assessing both quantita-

tive (number of seeds and plant species, cover of

vegetation) and qualitative ecosystem characteristics

(composition of seed bank and vegetation).

Materials and Methods

Study area

The study was conducted in a subalpine grassland

ecosystem (Alp Stabelchod) within the Swiss

National Park (SNP). The Park was founded in 1914

and is located in the south-eastern part of Switzer-

land (46!40¢N, 10!15¢E). It covers an area of

170 km2 ranging in altitude from 1400 to 3170

above sea level. Subalpine grasslands occupy only

3 km2 of the Park and are remarkable elements of

the landscape in the otherwise monotonous pine

(Pinus montana Miller) forests (Risch et al. 2003).

These grasslands are important grazing sites for red

deer (Cervus elaphus L.) during the summer months

(Schutz et al. 2003, 2006).

Alp Stabelchod (10.7 ha) is located at an elevation

of 1950 m and has a uniform slope of 6! in south-

erly direction. The mean annual temperature and

precipitation are 0.2!C ! 0.76 (mean ! SD), and

925 mm ! 162 (recorded at the Park’s weather sta-

tion Buffalora at 1977 m since 1917). The growing

season is from early June to the end of September.

Two vegetation types dominate on Alp Stabelchod,

which can be recognized easily: as a result of inten-

sive grazing by red deer, the vegetation height of the

herbaceous plant species rich short-grass type is

Ant–plant interactions in grassland ecosystems M. Schutz et al.

296J. Appl. Entomol. 132 (2008) 295–305 ª 2008 The Authors

Journal compilation ª 2008 Blackwell Verlag, Berlin

approximately 2 cm; the tall-grass type, which is

dominated by graminoids (mostly Carex sempervirens

Vill. tussocks), in contrast, exceeds 20 cm in vegeta-

tion height.

Ant mound abundance and distribution

A grid of 268 cells (20 m · 20 m) encompasses the

entire grassland of Alp Stabelchod (Achermann

2000), which we used for our study. Abundance and

distribution of mounds of F. exsecta are known from

a survey conducted on this grassland in 1998, when

mounds were counted and mapped in each of the

268 grid cells (Maggini 1999). F. exsecta is a common

species inhabiting grasslands of the SNP and in its

surrounding, the Engiadina valley (Kutter 1975;

Maggini et al. 2002). It inhabits open or slightly

shaded areas from heathland and grassland to forest

edges and clearings. The species shows its presence

by dome-shaped nests, which are usually composed

of pieces of grass litter. In areas where grass material

is not avaiable needles of coniferous trees or small

pebbles are used (Seifert 2000). Whereas monogy-

nous (one queen per nest) and monodomous (one

nest) populations are reported from e.g. southern

Finland (Seifert 2000), Swiss populations seem gen-

erally to be polygynous and polydomous (Kutter

1977). In our study area, ant mounds were found in

173 of the 268 grid cells on Alp Stabelchod, overall

757 mounds were recorded. The ant mounds

showed a distinct spatial pattern with higher densi-

ties in the tall-grass vegetation type (northern part,

western edge and southern part of the grassland)

and only few mounds in the central and eastern part

of the grassland where short-grass vegetation domi-

nated (Maggini 1999). The highest mound densities

(up to 23 mounds per gridcell or one mound per

17 m2) were found close to the forest edges where

the mounds were also larger than those far away

from the forest (Maggini 1999). Based on the infor-

mation obtained from this survey, we selected 24

grid cells for studying seed bank patterns of both ant

mounds and grassland soils.

Grassland soil and ant mound seed bank patterns

Grassland soil and ant mound cores were collected

in 24 randomly selected cells that contained at mini-

mum one ant mound (fig. 1). Seven grassland soil

cores (4.8 cm diameter, 10 cm depth) including both

the litter and mineral soil layer were systematically

taken with a core sampler along a 20 m transect

located 2 m from the western edge of each of the 24

grid cells. Two ant mound cores of 200 ml each were

taken from the mound that was located closest to

the grid cell centre and pooled. The seven grassland

soil cores of a grid cell were also pooled and sieved

through a 4 mm sieve to remove rocks and coarse

roots. We took roughly three times more grassland

soil than ant mound material (1260 vs. 400 ml), as

previous studies have shown that soil samples con-

tained between 30–37% rocks and 5–43% roots

(Risch 2004; Risch et al. 2005). After sieving, the

individual grassland soil samples averaged 494 ml.

All soil in access to 400 ml of each sample was then

taken to assess soil bulk density. All the cores were

collected immediately after snowmelt at the end of

May 2006, assuring that the seeds were stratified

during the previous winter.

The samples were spread in thin layers (<1 cm) on

trays filled with sterilized woody substrate serving as

moisture reservoir. The trays were randomly placed

on shelves in a green house chamber and their

Fig. 1 Schematic diagram of the study area Alp Stabelchod with the

experimental setup of 268 gridcells (20 m · 20 m). Black cells indicate

the random sample where grassland soil cores and cores of Formica

exsecta Nyl mounds were taken for the seed bank experiment.

M. Schutz et al. Ant–plant interactions in grassland ecosystems


positions were randomly changed every second

week to prevent microclimatic effects on seed germi-

nation. The trays were illuminated with natural

light, shaded from bright sunlight and watered daily

with tap water. Five additional trays containing only

woody substrate were used as a control to test for

seed contamination of the substrate. However, no

seedlings germinated in the control trays.

Seedlings were counted and identified [Lauber

and Wagner (1996) for nomenclature] as soon after

germination as possible and were then removed

from the trays. At the end of September 2006 all

samples were crumbled and remained spread out in

the tray for another 2 months to enable buried seeds

to germinate. No attempt was made to assess the

number of dormant seeds possibly remaining in the

samples.

Grassland and ant mound vegetation pattern

Vegetation data was sampled in 36 grid cells located

along two transects crossing Alp Stabelchod from

north to south (length = 460 m) and from east to

west (length = 280 m) respectively (fig. 2a). We

found a total of 46 ant mounds with diameter

>50 cm in these grid cells. On each of these

mounds we sampled vegetation data by establishing

two transects in northern/southern and eastern/

western direction through the centre (fig. 2b). We

conducted 13 circular (diameter = 30 cm) vegetation

releves per mound along these two transects: one

releve in the mound centre, four releves at the

mound’s edge, four at distance of 50 cm and four

at a distance of 100 cm from the mound’s edge

(fig. 2b). Plant species were identified within each

releve plot and the cover (%) of each species was

estimated following the method of Braun-Blanquet

(1964).

Statistical analysis

We defined a set of qualitative and quantitative

parameters based on the seed bank and vegetation

data collected. As quantitative parameters we chose:

(i) number of seeds per square metre of grassland/

ant mound surface, (ii) cover (%) of vegetation and

(iii) number of species in both the grassland and ant

mound seed bank and vegetation, while qualitative

parameters included individual plant species as well

as plant species groups defined by systematic or

functional classification: (i) graminoids (Poaceae, Cy-

peraceae, Juncaceae), (ii) legumes (Fabaceae), (iii)

dwarf shrubs (mainly Ericaceae) and (iv) myrmeco-

chors, i.e. species that are supposed to be adapted to

dispersal by ants. The classification of myrmecochor-

ous species followed Sernander (1906), Ulbrich

(1939), Muller-Schneider (1977, 1986) and Grime

et al. (1988).

Fig. 2 Schematic diagram of the

study area Alp Stabelchod with the

experimental setup of 268 gridcells

(20 m · 20 m): (a) checkered cells

indicate gridcells where vegetation

releves were conducted, (b) design

of the vegetation releve transects

and the releves conducted on all

ant mounds with diameter >50 cm

detected within a grid cell.




We used non-parametric tests (SPSS 11.0.4,

Chicago, Illinois, USA) to compare all quantitative

and qualitative variables of: (i) grassland and ant

mound seed bank and (ii) the vegetation along tran-

sects from ant mound centres into the grassland. The

seed bank variables (grassland vs. ant mound) were

compared with Wilcoxon’s signed rank test and the

vegetation variables (mound centre vs. mound edge

vs. 50 cm and vs. 100 cm from mound edge) with

Friedman’s test followed by Wilcoxon’s signed rank

test for pairwise comparison.

Results

Grassland soil and ant mound seed bank patterns

Overall, seedlings from 53 different plant species

emerged from the grassland and ant mound seed

bank samples. Thirty plant species were found in

both the grassland and ant mound samples, 11 spe-

cies in the grassland and 12 species in the ant

mound samples only. The average number of species

per sample was significantly different (P = 0.002)

between the grassland and mound samples with

nine compared with 12 species respectively (fig. 3a).

We found on average over 22 000 seeds/m2 in ant

mound material, which was 15 times more then the

1480 seeds/m2 in the grassland samples (P < 0.001,

fig. 3b). The number of seeds of myrmecochorous

species was only eight times higher in ant mound

compared with grassland material (1498 vs.

189 seeds/m2). Seeds of two plant species were more

abundant in the grassland seed bank than in the ant

mound samples whereas for 13 species the opposite

was true (table 1). Proportions of all four plant spe-

cies groups (graminoids, myrmecochors, legumes

and dwarf shrubs), however, were not significantly

different between grassland and ant mound material

(P > 0.05, fig. 4a–d).

Grassland and ant mound vegetation patterns

Overall, we found 92 different plant species in the

vegetation releves conducted on and around the ant

mounds: 15 plant species in the centre of ant

mounds, 77 at the mound edges, 85 at a distance of

50 cm and 83 at a distance of 100 cm from mound

edges. All 15 species from the centre were also found

in the other three locations and from the 77 species

found at mound edges, 74 were also found at a dis-

tance of 50 cm as well as 100 cm from mound edges.

The average number of species per releve consider-

ably differed along the transects (P < 0.001, fig. 5a):

Species richness increased from one species (median)

Fig. 3 Comparison of quantitative

parameters between 24 paired gra-

ssland and ant mound seed bank

samples respectively. Wilcoxon’s

signed rank tests was applied for

pairwise comparison: (a) number

of plant species (P = 0.002), b)

number of seeds/m2 (P < 0.001).

Box plots indicate median, 25th

and 75th percentiles, whiskers

10th and 90th percentiles and

black dots all values below 10th

and above 90th percentiles.

Table 1 Differentiating species between grassland and ant mound

seed bank samples

Wilcoxon’s signed rank test was applied for statistics (P < 0.05). Bold

numbers indicate significantly higher seed numbers.



per circular releve conducted in the centre of the ant

mounds to 21 species at the mound edges. Twenty-

six species were found at 50 cm, and 28.5 species

per releve at a distance of 100 cm from mound

edges. A similar pattern was detected for vegetation

cover (P < 0.001, fig. 5b) with 1% vegetation cover

(median) in the mound centre and 56%, 66%, to

69% vegetation cover at the edge, 50 and 100 cm

Fig. 4 Comparison of qualitative

parameters (species composition)

between 24 paired grassland and

ant mound seed bank samples

respectively. Wilcoxon’s signed

rank tests was applied for pairwise

comparison: proportions (%) of

(a) graminoids (P = 0.07),

(b) myrmecochors (P = 0.96),

(c) legumes (P = 0.97), (d) dwarf

shrubs (P = 0.10). Box plots

indicate median, 25th and 75th

percentiles, whiskers 10th and

90th percentiles and black dots all

values below 10th and above 90th

percentiles. Note that scales of

proportion axis are partly different.

Fig. 5 Comparison of quantitative vegetation parameters of transects from 46 ant mound centres into the grassland. Friedman’s test (P < 0.001

for all parameters) followed by Wilcoxon’s signed rank test was applied for pairwise comparison: (a) number of plant species, (b) vegetation cover

(%). Different letters indicate statistical differences (P < 0.05) between samples. Box plots indicate median, 25th and 75th percentiles, whiskers

10th and 90th percentiles and black dots all values below 10th and above 90th percentiles.




distance respectively. The abundance of 51 of the 92

plant species significantly differed (P < 0.05) along

the vegetation transects through ant mounds

(table 2). A similar pattern was found for the four

plant species groups (P < 0.001 for all comparisons,

fig. 6a–d). When a plant species was found in a

releve conducted in the ant mound centres it was

most often a graminoid (median = 100%, fig. 6a).

The proportion of graminoids decreased to 35% at

the edges of the mounds, 29.6% at a distance of

50 cm and to 27.6% at a distance of 100 cm from

mound edges. In contrast, the proportion of myr-

mecochorous plant species increased from the

mound centres into the grassland: 0% were found in

the centres, 12.5%, 13.6% and 14% in the other

three locations respectively. A median of 0% was

also found for legumes in the mound centres

(fig. 6c). The abundance of legumes was higher in

the three other locations compared with the mound

centre, but did not differ between these three loca-

tions (mound edge = 8.5%, 50 cm from

edge = 8.3%, 100 cm from edge = 7.9%). Yet

another pattern was found for dwarf shrubs

(fig. 6d): the highest proportion of seeds were

recorded for the edge of ant mounds (4.4%) fol-

lowed by grassland releves (3.3–3.4%) and releves

from the ant mound centres (0%).

Discussion

Effects of ants on seed bank and vegetation patterns

We found a considerable impact of F. exsecta on

seed bank and vegetation patterns in the grassland

ecosystem studied. Ants of each single mound

altered grassland patterns in both quantitative and

qualitative aspects. We found on average 15 times

more seeds, eight times more myrmecochors and

slightly higher species richness in the ant mound

compared with grassland seed bank samples. Simi-

larly, Dauber et al. (2006) reported twice as many

seeds in ant mounds of Lasius flavus Fabricius com-

pared with soil samples in a German pasture,

whereas King (1976) found slightly lower number

of seeds in mounds of the same ant species in Brit-

ish grasslands. Also Dostal (2005) detected only half

the number of seeds in ant mounds of Tetramorium

caespitum L. than in soil samples collected in a Slo-

vakian grassland.

Our results also showed that in contrast to seed

density in the seed bank, the seed bank composi-

tion was very similar between ant mound and

grassland samples. To our surprise, we did not find

any difference in the proportion of myrmecochor-

ous seeds between the two-seed bank communities,

even though many studies reported that ants pre-

ferred collecting myrmecochorous seeds with elaio-

soms (Sernander 1906; King 1976; Abramsky 1983;

Van Tooren 1988; Hughes and Westoby 1992;

Mark and Olesen 1996; Gorb et al. 2000; Gorb and

Gorb 2003; Dostal 2005; Dauber et al. 2006). How-

ever, it has also been shown for several ant species

that they discard seeds outside their mounds (Beat-

tie 1985; Dostal 2005) or at the border of the terri-

tory (Gorb et al. 2000) after removing the

elaiosoms and feeding them to their larvae. This

behaviour could likely explain the patterns of myr-

mecochorous plants we found in our study, as the

proportion of myrmecochorous plant species in the

vegetation increased with increasing distance from

the centre of the mounds. This would also lead to

higher seed production and seed rain of myrmec-

ochorous species outside compared with on the

mounds. The seed production and rain of grami-

noid species in contrast, would be exactly opposite

to this pattern as we found more graminoids grow-

ing on/close opposed to outside the mounds. Con-

sequently, it is possible that we underestimated the

importance of F. exsecta in collecting myrmecochor-

ous seeds, as collecting seeds from distant sources

requires more work. Similarly, we possibly overesti-

mated the importance of ants in collecting grami-

noid seeds.

The different growth forms of many graminoid

species compared with most herbaceous species

could likely explain the dominance of graminoids

on ant mounds. Lesica and Kannowski (1997)

reported that mainly rhizomatous graminoids are

able to grow on active ant mounds of several

mound-building ant species in peatlands in the

USA.

Further, our results indicate that seed predation

probably is of minor importance for F. exsecta as

high number of seeds was found within the

mounds that probably accumulated over several

years and remained viable in the mounds (Beattie

1985). In addition, accumulation of seeds could be

a result of seed protection against predation from

within the mounds (Turnbull and Culver 1983;

Gibson 1993; Manzaneda et al. 2005). We think

that instead of consuming the seeds, the ants use

them for mound construction, a behaviour that

also has been reported for the mound-building red

wood ant Formica polyctena Forster in

deciduous forests of the Ukraine (Gorb and Gorb

2003).



Table 2 Significantly differentiating species (mean cover %) of the vegetation transects conducted from ant mound centres into the grassland

Friedman’s test (v2 and P < 0.05 indicated in table) followed by Wilcoxon’s signed rank test for pairwise comparison was applied for statistics. Bold

numbers indicate significantly higher species cover.




Effect of ants on spatial patterns at the ecosystem

scale

Our results showed that the ants have a considerable

impact on the seed bank and vegetation patterns

around the mounds. However, taking the high den-

sity of on average almost 70 mounds per ha found

on Alp Stablechod into account, we suggest that the

impact of these insects is not restricted to the closest

surroundings of mounds, but affects the entire grass-

land ecosystem. Also data by Achermann (2000) and

Maggini (1999) suggest such larger scale effects of

F. exsecta on ecosystem processes on Alp Stabelchod.

These authors found that grazing patterns of red

deer were highly negatively correlated with ant

mound densities. Four different mechanisms may

explain these patterns and support our hypothesis

that F. exsecta influence the entire grassland: (i) the

ants seem to favour the growth of graminoids on

and around the mounds compared with herbaceous

plants, which are more frequently found in areas

grazed by ungulates (Schutz et al. 2000, 2003; Nash

et al. 2001); (ii) the impact of herbivores may be

indirect by removing vegetation that the ants would

need as nesting material or for nutrition (Beever and

Herrick 2006; Bliss et al. 2006); (iii) the ants behave

aggressively against sources of disturbance such as

herbivores (Kutter 1975), thus the ungulates tend to

avoid areas with high ant mound densities; (iv) large

grazing herbivores are a major disturbance agent for

the ant mounds (e.g. trampling) and displace the

ants directly into grassland parts where herbivores

do not graze intensively because of lower nutritional

quality of the forage (James et al. 1999). For exam-

ple, King (1981) showed that the period since the

last disturbance in calcareous grasslands was highly

correlated with mound size and activity of L. flavus.

We conclude that F. exsecta not only altered grassland

characteristics in the close surrounding of their

mounds, but that they affect the entire grassland.

Moreover, these ants might be important drivers in

creating heterogeneity in ecosystem patterns such as

the spatial use of the grassland by red deer.

Acknowledgements

We thank Dieter Trummer for his assistance in the

field, Werner Lauchli who took care of the green-

Fig. 6 Comparison of qualitative

vegetation parameters (species

composition of transects from 46

ant mound centres into the grass-

land. Friedman’s test (P < 0.001 for

all parameters) followed by

Wilcoxon’s signed rank test was

applied for pairwise comparison.

Proportions (%) of: (a) graminoides,

(b) myrmecochors, (c) legumes and

(d) dwarf shrubs. Different letters

indicate statistical differences

(P < 0.05) between samples. Box

plots indicate median, 25th and

75th percentiles, whiskers 10th

and 90th percentiles and black

dots all values below 10th and

above 90th percentiles. Note that

scales of proportion axis are partly

different.



house experiments and two unknown reviewers for

their helpful comments. We are grateful for the sup-

port by the Swiss National Park administration.

References

Abramsky Z, 1983. Experiments on seed predation by

rodents and ants in the Israeli desert. Oecologia 57,

328–332.

Achermann G, 2000. The influence of red deer (Cervus

elaphus L.) upon a subalpine grassland ecosystem in the

Swiss National Park. PhD. thesis ETH 13479, Zurich.

Andersen AN, Sparling GP, 1997. Ants as indicators of

restoration success: relationship with soil microbial bio-

mass in the Australian seasonal tropics. Restor. Ecol. 5,

109–114.

Bakker ES, Olff H, 2003. The impact of different-sized

herbivores on recruitment opportunities for subordi-

nate herbs in grasslands. J. Veg. Sci. 14, 465–474.

Bantzing W, 1996. Landwirtschaft im Alpenraum-un-

verzichtbar aber zukunftslos: Eine alpenweite Bilanz

der aktuellen Probleme und der moglichen Losungen.

Blackwell, Berlin.

Bazzaz FA, 1996. Plants in changing environments: link-

ing physiological, population, and community ecology.

Cambridge University Press, Cambridge.

Beattie AJ, 1985. The evolutionary ecology of ant-plant

mutualisms. Cambridge University Press, Cambridge.

Beever EA, Herrick JE, 2006. Effects of feral horses in

Great Basin landscapes on soils and ants: direct and

indirect mechanisms. J. Arid Environm. 66, 96–112.

Bliss P, Katzerke A, Neumann P, 2006. The role of mole-

hills and grasses for filial nest founding in the wood

ant Formica exsecta (Hymenoptera: Formicidae). Sociobi-

ology 47, 903–913.

Braun-Blanquet J, 1964. Vegetation ecology: the study of

plant communities. Hafner, London.

Dauber J, Rommeler A, Wolters V, 2006. The ant Lasius

flavus alters the viable seed bank in pastures. Eur. J.

Soil. Biol. 42, 157–163.

Davidson DW, Morton SR, 1981. Myrmecochory in some

plants (F. Chenopodiaceae) of the Australian arid zone.

Oecologia 50, 357–366.

Dean WRJ, Milton SJ, KKlotz S, 1997. The role of ant

nest-mounds in maintaining small-scale patchiness in

dry grasslands in Central Germany. Biodivers. Conserv.

6, 1293–1307.

Dostal P, 2005. Effect of three mound-building ant spe-

cies on the formation of soil seed bank in mountain

grassland. Flora 200, 148–158.

Fenner M, Thompson K, 2005. The ecology of seeds.

Cambridge University Press, Cambridge.

Folgarait PJ, 1998. Ant biodiversity and its relationship to

ecosystem functioning: a review. Biodivers. Conserv. 7,

1221–1244.

Forget P-M, Lambert JE, Hulme PE, Van der Wall SB,

2005. Seed fate. Predation, dispersal and seedling

establishment. CABI Publishing, Wallingford.

Gibson W, 1993. Selective advantages to hemi-parasitic

annuals, genus Melampyrum, of a seed-dispersal

mutualism involving ants: II. Seed-predator avoidance.

Oikos 67, 345–350.

Gorb EV, Gorb SN, 2003. Seed dispersal by ants in a

deciduous forest ecosystem: mechanisms, strategies,

adaptations. Kluwer, Dordrecht.

Gorb SN, Gorb EV, Sindarovskaya Y, 1997. Interaction

between the non-myrmecochorous herb Galium aparine

and the ant Formica polyctena. Plant Ecol. 131, 215–221.

Gorb SN, Gorb EV, Puntilla P, 2000. Effects of redispersal

of seeds by ants on vegetation pattern in a deciduous

forest: a case study. Acta Oecol. 21, 293–301.

Grime JP, Hodgson JG, Hunt R, 1988. Comparative plant

ecology. Hyman, London.

Handel SN, 1978. The competitive relationship of three

woodland sedges, and its bearing on the evolution of ant

dispersal of Carex pedinculata. Evolution 32, 151–163.

Holldobler B, Wilson EO, 1990. The ants. Harvard Uni-

versity Press, Cambridge.

Hughes L, Westoby M, 1992. Effect of diaspore character-

istics on removal of seeds adapted for dispersal by ants.

Ecology 73, 1300–1312.

James CD, Landsberg J, Morton SR, 1999. Provision of

watering points in the Australian arid zone: a review

of effects on biota. J. Arid Environ. 41, 87–121.

Kelrick MI, MacMahon JA, Parmentier RR, Sisson DV,

1986. Native seed preference of shrup-steppe rodents,

birds and ants: the relationships of seed attributes and

seed use. Oecologia 68, 327–337.

King TJ, 1976. The viable seed content of ant-hill and

pasture soil. New Phytol. 77, 143–148.

King TJ, 1981. Ant-hills and grassland history. J. Bio-

geogr. 8, 329–334.

Kozlowski TT, 1972. Seed biology I. Academic Press, Lon-

don.

Kutter H, 1975. Die Ameisen (Hym. Formicidae) des

Schweizerischen Nationalparkes und seiner Umgebung.

Ergebn. Wiss. Untersuch. Schweiz. Nat. Park 14, 398–

414.

Kutter H, 1977. Formicidae – Hymenoptera, Insecta Hel-

vetica 6. Schweizerische Entomologische Gesellschaf,

Zurich.

Lauber K, Wagner G, 1996. Flora Helvetica. Haupt, Bern.

Lesica P, Kannowski PB, 1997. Ants create hummocks

and alter structure and vegetation of a Montana fen.

Am. Midl. Nat. 139, 58–68.

Maggini R, 1999. Etude de la distribution de Formica ex-

secta Nyl. (Hymenoptera: Formicidae) au Parc national

Suisse a l’aide d’un Systeme d’Information Geographi-

que (SIG) . Travail de diplome, University of Lausanne,

Lausanne.




Maggini R, Guisan A, Cherix D, 2002. A stratified

approach for modelling the distribution of a threatened

ant species in the Swiss National Park. Biodivers.

Conserv. 11, 2117–2141.

Malo JE, Suarez F, 1995a. Establishment of pasture spe-

cies on cattle dung: the role of endozoochorous seeds.

J. Veg. Sci. 6, 169–174.

Malo JE, Suarez F, 1995b. Herbivorous mammals as seed

dispersers in a Mediterranian pasture. Oecologia 104,

246–255.

Manzaneda AJ, Fedriani JM, Rey PJ, 2005. Adaptive

advantages of myrmecochory: the predator-avoidance

hypothesis tested over a wide geographic range.

Ecography 28, 583–592.

Mark S, Olesen JM, 1996. Importance of eleiosome size

to removal of ant-dispersed seeds. Oecologia 107, 95–

101.

Mittelbach GG, Gross KL, 1984. Experimental studies of

seed predation in old fields. Oecologia 56, 109–116.

Mouissie AM, Vos P, Verhagen HMC, Bakker JP, 2005.

Endozoochory by free-ranging, large herbivores: eco-

logical correlates and perspectives for restoration. Basic

Appl. Ecol. 6, 547–559.

Muller-Schneider P, 1977. Verbreitungsbiologie (Diaspo-

rologie) der Blutenpflanzen. Veroff. Geobot. Inst. ETH

61, 3–226.

Muller-Schneider P, 1986. Verbreitungsbiologie der

Blutenpflanzen Graubundens. Veroff. Geobot. Inst.

ETH 85, 3–261.

Myers JA, Vellend M, Gardescu S, Marks PL, 2004. Seed-

dispersal by white-tailed deer: implications for long-dis-

tance dispersal, invasion, and migration of plants in

eastern North America. Oecologia 139, 35–44.

Nash MS, Whitford WG, Bradford DF, Franson SE, Neale

AC, Heggem DT, 2001. Ant communities and livestock

grazing in the Great Basin, U.S.A. J. Arid Environ. 49,

695–710.

Nathan R, Muller-Landau HC, 2000. Spatial patterns of

seed dispersal, their determinants and consequences

for recruitment. Trends Ecol. Evol. 15, 278–285.

Oostermeijer JGB, 1989. Myrmecochory in Polygala

vulgaris L., Luzula campestris (L.) D.C. and Viola

curtisii Forster in a Dutch dune area. Oecologia 78,

302–311.

Pakeman RJ, Engelen J, Attwood JP, 1999. Rabbit endo-

zoochoriy and seedbank build-up in an acidic grass-

land. Plant Ecol. 145, 83–90.

Pakeman RJ, Digneffe G, Small JL, 2002. Ecological cor-

relates of endozoochory by herbivores. Func. Ecol. 16,

296–304.

Retana J, Pico XF, Rodrigo A, 2004. Dual role of

harvesting ants as seed predators and dispersers of a

non-myrmecochorous Mediterranean perennial herb.

Oikos 105, 377–385.

Risch AC, 2004. Above- and belowground patterns and

processes following land use change in subalpine coni-

fer forests of the Central European Alps. PhD. thesis

ETH 15368, Zurich.

Risch AC, Nagel LM, Schutz M, Krusi BO, Kienast F,

Bugmann H, 2003. Structure and long-term develop-

ment of subalpine Pinus montana Miller and Pinus cem-

bra L. forests in the central European Alps. Forstwiss.

Cbl. 122, 219–230.

Risch AC, Jurgensen MF, Schutz M, Page-Dumroese DS,

2005. The contribution of red wood ants on soil C and

N pools and CO2 emissions in subalpine forests. Ecol-

ogy 86, 419–430.

Schutz M, Wildi O, Krusi BO, Marki K, Nievergelt B,

2000. From tall-herb communities to pine forests: dis-

tribution patterns of 121 plant species during a 585-

year regeneration process. Nat.park Forsch. Schweiz

89, 237–255.

Schutz M, Risch AC, Leuzinger E, Krusi BO, Achermann

G, 2003. Impact of herbivory by red deer (Cervus ela-

phus L.) on patterns and processes in subalpine grass-

lands in the Swiss National Park. Forest Ecol. Manage.

181, 177–188.

Schutz M, Risch AC, Achermann G, Thiel-Egenter C,

Page-Domroese DS, Jurgensen MF, Edwards PJ, 2006.

Phosphorus translocation by red deer on a subalpine

grassland in the Central European Alps. Ecosystems 9,

624–633.

Seifert B, 2000. A taxonomic revision of the ant subge-

nus Coptoformica Mueller, 1923 (Hymenoptera, Formici-

dae). Zoosystema 22, 517–568.

Sernander R, 1906. Entwurf einer Monographie der

europaischen Myrmekochoren. Kunglica Svenska

Vetenskapsakademiens Handlingar 41, 1–410.

Tackenberg O, Poschlod P, Bonn S, 2003. Assessment of

wind dispersal potential in plant species. Ecol. Monogr.

73, 191–205.

Tasser E, Walde J, Tappeiner U, Teutsch A, Noggler W,

2007. Land-use changes and natural reforestation in

the Eastern Central Alps. Agr. Ecosyst. Environ. 118,

115–129.

Turnbull CL, Culver DC, 1983. The timing of seed dis-

persal in Viola muttallii: attraction of dispersers and

avoidance of predators. Oecologia 59, 360–365.

Ulbrich E, 1939. Deutsche Myrmekochoren: Beobachtun-

gen uber die Verbreitung heimischer Pflanzen durch

Ameisen. Fischer, Berlin.

Van Tooren BF, 1988. The fate of seeds after dispersal in

chalk grassland: the role of bryophyte layer. Oikos 53,

41–48.

Welch D, 1985. Studies in the grazing of heather moor-

land in North-East Scotland. IV Seed dispersal and

plant establishment in dung. J. Appl. Ecol. 22, 461–

472.



Impact of Formica exsecta Nyl. on seed bank and vegetation patterns in a subalpine grassland...

Documents

Transcript of Impact of Formica exsecta Nyl. on seed bank and vegetation patterns in a subalpine grassland...