Download Influence of driver ant swarm raids on earthworm prey densities in

Insect. Soc. (2010) 57:73–82
DOI 10.1007/s00040-009-0052-y
Insectes Sociaux
RESEARCH ARTICLE
Influence of driver ant swarm raids on earthworm prey densities
in the Mount Kenya forest: implications for prey population
dynamics and colony migrations
C. Schöning • C. Csuzdi • W. Kinuthia
J. O. Ogutu
•
Received: 30 March 2009 / Revised: 9 October 2009 / Accepted: 21 October 2009 / Published online: 8 November 2009
Ó Birkhäuser Verlag, Basel/Switzerland 2009
Abstract African driver ants are nomadic social mesopredators feeding on a highly diverse array of prey species
at different trophic levels. Colonies of certain driver ant
species have a biomass which can equal that of mediumsized mammalian carnivores and the ultimate cause of their
nomadic life-style is thought to be local prey depletion.
The impact of driver ant swarm raids is therefore expected
to be strong but the degree to which they reduce prey
populations has not been quantified and it is unknown
whether these spectacular predators exert significant topdown effects. We examined the combined effect of driver
ant (Dorylus molestus) and swarm-attending bird (Alethe
poliocephala) predation on the population dynamics of
earthworms, which constitute the ants’ main prey type in
Electronic supplementary material The online version of this
article (doi:10.1007/s00040-009-0052-y) contains supplementary
material, which is available to authorized users.
C. Schöning (&)
Department of Biology, Centre of Social Evolution,
University of Copenhagen, Universitetsparken 15,
2100 Copenhagen, Denmark
e-mail: [email protected]
C. Schöning
Länderinstitut für Bienenkunde,
Friedrich-Engels-Strasse 32,
16540 Hohen Neuendorf, Germany
C. Csuzdi
Systematic Zoology Research Group of Hungarian
Academy of Sciences, Budapest, Hungary
C. Csuzdi
Department of Zoology,
Hungarian Museum of Natural History,
P.O. Box 137, 1431 Budapest, Hungary
the montane forest of Mount Kenya. Pre-raid earthworm
biomass densities in the soil layer down to a depth of 8 cm
varied by a factor of 31. The immediate effect of swarm
raids was a reduction in earthworm numbers in this layer,
but 8 days later earthworm numbers had recovered to preraid levels. When earthworm biomass densities were
compared, no significant effect of swarm raids was detected. The estimated proportion of earthworm prey biomass
extracted from 0 to 8 cm layer by driver ants and birds
together was about 2.2%. Although colony distribution
was overdispersed as expected based on knowledge of
D. molestus migratory behaviour, predation events were
highly localized. Predation frequency was low (once every
62 days on average) and highly variable. These results
indicate that earthworm prey is highly abundant but at the
same time so difficult to harvest that swarm raids exert only
a marginal influence on earthworm populations. Longerterm studies would be required to determine whether
W. Kinuthia
Department of Invertebrate Zoology,
National Museums of Kenya, 40658,
00100 Nairobi, Kenya
J. O. Ogutu
International Livestock Research Institute,
30709, 00100 Nairobi, Kenya
J. O. Ogutu
Universität Hohenheim,
Institut für Pflanzenbau und Grünland,
Fruwirthstrasse 23,
70599 Stuttgart-Hohenheim, Germany
74
earthworm populations are limited by swarm raids. The
small impacts of individual raids and rapid recovery of
earthworm prey populations likely underlie the low frequency of migrations and short distances travelled by
migrating colonies of D. molestus.
Keywords Ant-following birds Army ants Dorylus molestus Nomadism
Introduction
Terrestrial carnivores can have strong direct effects on the
structure and dynamics of prey communities via predator–
prey interactions (Sih et al., 1985; Schoener and Spiller,
1996; Frank, 2008; Dunham, 2008). Such effects can cascade beyond the prey base to lower trophic levels (Schmitz,
2003; Terborgh et al., 2001). If the effects of predation are
strong and density-dependent, then carnivores can limit the
population growth of prey species occurring at low densities
and constituting their primary food source in environments with few suitable alternative prey species (Sinclair,
2003).
Driver ants [Dorylus (subgenus Anomma) spp.; Savage,
1847; see also Kronauer et al., 2007] hunt by massive
swarm raids on the forest floor and up in the vegetation in
which hundreds of thousands or even a few million ant
workers form a dense carpet that sweeps through areas of
up to 1,000 m2 or more in a single day (Leroux, 1982).
Such raid swarms can be 20 m or more wide (Leroux,
1982) and attract birds feeding on animals attempting to
escape from the marauding ants (Keith et al., 1992; Peters
et al., 2008). Colonies of the West African species Dorylus
nigricans may contain as many as 7 million adult workers
and have a total fresh mass of 50 kg (Leroux, 1982) which
is equivalent to that of a female leopard (Kingdon, 1997).
Driver ants have an extremely wide prey spectrum,
ranging from solitary insects (mostly immature stages),
Annelida (earthworms), Myriapoda (millipedes and centipedes), Crustacea (crabs, woodlice), Gastropoda (slugs and
snails), Arachnida (spiders, harvestmen) to large social
insect colonies (ants, honey bees), occasionally even
including vertebrates (snakes, frogs, mammal carcasses)
(Savage, 1847; Gotwald, 1995; Schöning et al., 2008). Thus,
they affect prey species at many different trophic levels and
in both aboveground and belowground food webs. Several
vertebrates such as chimpanzees, mongooses and pangolins
as well as subterranean army ants of the subgenus Dorylus
(Typhlopone) feed on driver ants (Gotwald, 1995; Kingdon,
1997), so that they are not top predators. Colonies often
move to new nest sites and the ultimate cause for these
migrations is thought to be local prey depletion (Wilson,
1958; Gotwald, 1995).
C. Schöning et al.
Although several authors have inferred that driver ants
have an intense impact on or may even limit populations of
their prey (e.g. Vosseler, 1905; Weber, 1943; Dejean et al.,
1999), to date no study has quantified the amounts of
harvested prey in relation to their availability or examined
the length of time necessary for prey populations to recover
to original levels following raids. Moreover, the spatiotemporal patterns of driver ant raids at the habitat level
have not yet been thoroughly documented. However, data
on these phenomena are essential for understanding the
influence of driver ant predation on the population
dynamics and diversity of aboveground and belowground
invertebrate communities in African forests and for elucidating the evolution of the nomadic habits of driver ants.
While the nomadic patterns of the neotropical swarmraiding ant Eciton burchellii are highly stereotypical
(Franks and Fletcher, 1983), migrations of driver ant colonies occur at irregular and much lower frequencies
(Gotwald, 1995; Schöning et al., 2005a).
Here we analyse the predator–prey relationship between
the driver ant Dorylus molestus and earthworms. Earthworms are an important prey for many driver ant species
(Gotwald, 1974; Schöning, unpubl. data) and represent the
ants’ main food type at our study site in the montane forest
of Mount Kenya (Schöning et al., 2008). D. molestus is
widely distributed throughout eastern Africa (from Ethiopia to Mozambique) and searches for prey not only in the
leaf-litter, on the forest floor and up on the vegetation but
also intensely in the upper soil layers. During raids groups
of workers often stay behind when the advancing swarm
has passed and start digging. Minutes or hours later
earthworms surge out of these holes in usually unsuccessful
attempts to escape (see picture in Supplementary online
material) or are transported out of them in pieces.
The pivotal importance of earthworms in soil biology
has been well documented. In tropical rainforests they
represent about 50% of the biomass of the soil macrofauna
(Fragoso and Lavelle, 1992). Many studies have emphasized that earthworms are powerful regulators of soil
processes, contributing to the maintenance of soil structure
and the regulation of soil organic matter dynamics
(Lavelle, 1997; Brussaard, 1998). They mix organic and
mineral materials producing organo-mineral complexes
that influence soil structure and fundamental soil processes
such as carbon mineralization, nitrogen fixation, nitrification, and other processes (Hooper et al., 2000). They also
produce physical structures, like burrows, that are not only
essential in maintaining soil porosity but also constitute
specific sites of distinct soil processes (Perreault and
Whalen, 2006). Therefore, earthworms are considered to be
ecosystem engineers (Lavelle et al., 1997). Exclusion
experiments have shown that predation by birds and
mammals can have strong effects on earthworm
Impact of driver ant swarm raids on earthworms
populations in afrotropical forests (Dunham, 2008). When
predators keep earthworm population densities below carrying capacity, this might result in reduced leaf-litter
decomposition.
We compared the pre- and post-raid earthworm densities, estimated raid impact based on prey retrieval data and
examined the frequency and spatial pattern of raids. The
impact of individual raids on earthworm population density
was small and predation frequency was rather low but
highly variable. We discuss how predation by driver ants
and associated birds influences earthworm population
dynamics and examine implications of prey population
dynamics for driver ant migratory behaviour.
Study site and methods
75
Earthworm sampling plots samples taken at different times:
Raid swarm
Foraging trail
Nest
10m
Fig. 1 Scheme for sampling earthworms before, immediately after
and 8 days after driver ant predation. The sampling plots are squares
with a side length of 50 cm. Please note that plot locations were
actually slightly off-set because of the advance of the raid swarm
during the sampling of earthworm density before raids
Study site
The study was carried out in August 2007 and January–
February 2008 at the same site in the montane forest at the
eastern slope of Mount Kenya (0°140 S, 37°340 E, altitude
1,850 m a.s.l.) used by Schöning et al. (2005a, 2008).
The vegetation is classified as forest dominated by Octoea
usambarensis (Lauraceae), although the abundance of
this tree was reduced by selective logging in the past
(Bussmann 1994). Rainfall is bimodal with two rainy
seasons spanning March–May and October–December
(Supplementary online material). Mean annual rainfall at
Chogoria Forest Station (ca. 2.2 km from the study site)
was 2,178 mm during the period February 1973–March
2008. The soil at the study site has been classified as
dystric and humic nitrosols (‘‘area with dense small river
network: very deep, dark, red, friable clay; partly covered
by shallow, dark reddish brown, humic clay’’, Speck,
1983). Voucher specimens of the D. molestus driver ants
(species status: Gotwald, 1974) from this population were
deposited in the Zoological Museum of the University of
Copenhagen by Kronauer et al. (2006). Voucher specimens
of the earthworm species found in this study have been
deposited in the Oligochaeta collection of the Hungarian
Natural History Museum, Budapest (Reg. No. HNHM
AF/5227-5233).
Impact of swarm raids on earthworm density
We found swarm raids by daily monitoring of five randomly selected colonies. Once a raid swarm had been
located, we observed the area around the swarm from the
periphery for 15 min and noted the maximum number of
attending ant-following birds and their identity (Stevenson
and Fanshawe, 2002). The swarm front’s end points were
then marked with small flags so that its width could later be
measured using a metre-tape. At each raid swarm we
sampled nine 50 9 50 cm2 plots for earthworms: the first
three about 100 cm ahead of the swarm (original earthworm density), the second three plots about 100 cm behind
the swarm front (the positions of these plots were at first
only indicated with small flags; sampling was carried out
only after all foraging activity had ceased in the particular
area, this was usually the case after 1–4 h) and the last set
of plots in between the other plots 8 days later. Plot locations were selected as illustrated in Fig. 1. At each plot the
leaf-litter was collected and checked for earthworms before
a soil monolith (down to a depth of 8 cm) was dug up with
a spade and then hand-sorted for earthworms which were
killed and preserved in 70% ethanol. The earthworms from
the three plots per set were pooled. We chose a depth of
8 cm as previous observations had suggested that the ants
do not dig deeper (see ‘‘Discussion’’). Since many individuals were incomplete (either because they had been cut
by the spade used for digging or because they had autotomized), we determined the numbers of all earthworm
pieces and also their total biomass (after oven-drying at
60°C for 48 h). Earthworm densities were measured in this
way in August 2007 at five swarms each of five ant colonies. The reason for examining earthworm density 8 days
after the raids was that army ant migration frequency
depends on the recovery dynamics of prey populations
(Franks 2001) and recovery of populations of solitary
invertebrate species seems to take place within 1 week
(Franks 1980). Only those raid areas were re-sampled
8 days later for which we could unambiguously ascertain
by subsequent daily monitoring that no other swarm raid
took place in the area. For comparisons, earthworm prey
biomass density data were ln-transformed to better
approximate a normal distribution. Prey densities before,
immediately after and 8 days after raids were compared
76
C. Schöning et al.
with paired t tests. The critical p value was adjusted from
0.05 to 0.025 for experimentwise error using the Bonferroni method (Sokal and Rohlf, 1995). All reported p values
are for two-sided tests. To estimate the biomass range of
complete individual earthworm specimens available to the
ants, we additionally weighed several specimens at both
size extremes.
opportunistically collected earthworms captured in swarm
raids of the focal colonies on days when no other data or
samples were gathered from these colonies. The earthworm
specimens were preserved as described above for later
identification.
Independent estimation of swarm raid impact
based on prey composition and prey retrieval data
At the start of the fieldwork in January 2008, we delimitated a study area for measuring colony density without
prior knowledge of active nest locations by choosing as
border points conspicuous landmarks we remembered from
previous fieldwork. The northern and southern boundaries
were chosen to be a river and a dirt road, respectively. Over
the course of 14 days we intensively and exhaustively
surveyed the area systematically for the presence of colonies without leaving any area larger than 20 9 20 m2
unvisited. All detected colonies were subsequently monitored daily and the number of colonies nesting in the study
area at the end of the 14-day period was taken to represent
the total number of colonies. At the end of the 14-day
period all active nest locations and boundary points were
recorded with a Global Positioning System (GPS) receiver
(GarminÒ, Model Summit).
We also prepared a map based on bearing and distance
data measured by compass and metre tape in order to
validate the accuracy of the first method. The map created
from GPS data does not take into account the rugged
topography of the study site and may thus underestimate
distances and areal size. The spatial distribution of
D. molestus colonies in the map based on data measured by
compass and metre tape was examined by calculating the
univariate L-function (Ripley, 1976; Besag, 1977) using the
software PROGRAMITA (Wiegand and Moloney, 2004).
Ninety-nine Monte Carlo simulations were run to test
whether the observed L-values deviate from the null
hypothesis of complete spatial randomness at spatial scales,
r, ranging from 10 to 300 m.
As an independent estimate of the impact of swarm raids
on earthworm density we calculated the amounts of
earthworm prey extracted from hunting areas based on prey
composition and prey retrieval data. This is important
because our method comparing pre- and post-raid densities
does not allow distinguishing between earthworm individuals actually removed by ants and birds and those which
escaped (e.g. into deeper soil layers). Prey retrieval rates
were measured at exposed sections of the principal foraging trail close to the nest when the respective swarms were
fully developed. Two observers counted the number of
items carried towards the nest over a period of 10 min. The
mean of the numbers counted by the two observers was
calculated. We examined the prey composition of four prey
samples (n = about 200 items each) collected from each of
the same five colonies whose swarm raids were studied.
Prey samples were not collected on days when the impact
of swarm raids on earthworm density was examined. Items
were sorted into the two categories: earthworms and nonearthworm prey. Biomass (48 h at 60°C) of earthworm
prey and other prey types was determined for each of the
20 samples. The area from which prey was extracted over a
10-min period was estimated based on the mean swarm
raid width (see above) and the mean swarm raid speed of
7.2 m/h (Schöning et al., 2005a). Birds attending the
swarm have been observed to capture earthworms trying to
escape from the ants (either within or ahead of the swarm
raid area), so that the birds’ predatory activities also need
to be taken into account when assessing the impact of
swarm raids. The birds’ prey intake was estimated based on
knowledge of feeding energetics (see Franks, 1980, p. 81).
Identity of available and hunted earthworms
In February 2008, we sampled earthworms at 40 randomly
selected 50 9 50 cm2 plots but this time we hand-sorted
not only the 0–8 cm soil layer but also the 8–30 cm layer.
All the earthworm specimens collected in 2008 were first
killed in 70% ethanol, then kept in 5% methanal for 4 days
for fixation and subsequently stored in 70% ethanol. Later
in the laboratory the specimens were identified according
to Sims (1982) and their wet mass was determined. We also
Colony density and distribution
Spatial and temporal predation patterns
From January 30th to February 23rd, 2008, we used 100
pitfall traps placed along 4 straight transects with 25 traps
each (10 m distance between traps) to investigate how often
a given spot in the habitat is visited by a swarm raid and
how evenly predation events are spread. The transect start
points and directions had been chosen before the beginning
of the colony survey (see above). The pitfall traps (2.8 cm
inner diameter, ca. 10 cm deep) were placed into the soil so
that their upper ridges were flush with the soil surface. The
traps were 2/3 filled with a mixture of 60% propyl glycol, 5–
10% ethanol and 30–35% water. Earlier experiments (four
traps each placed ahead of the raid swarms of four colonies)
Impact of driver ant swarm raids on earthworms
showed that this method reliably recorded predation events
(all of the 16 traps contained ants). Traps were checked
daily for ants and the numbers of caught individuals
counted. Other organisms and debris were removed and
liquid was added as necessary.
Results
Impact of swarm raids on earthworm density
The average swarm raid width of 10.60 m (±3.52 m SD,
range 5.00–17.40 m, n = 25; Table 1) did not differ from
the one measured by Schöning et al. (2005a) (10.30 ±
4.60 m SD; t test, t = 0.27, df = 65, p = 0.79). Swarms
were attended on average by 1.4 birds (±1.12 SD, range 0–
4). All birds belonged to Alethe poliocephala (Bonaparte), a
species known to attend driver ant swarms regularly (Keith
et al., 1992; Peters et al., 2008). There was no significant
relationship between swarm width and number of attending
birds (Spearman, r = 0.13, ns, n = 25).
No earthworms were found in the leaf-litter. The mean
original earthworm density was 34.92 pieces (±19.13 SD,
range 7–75, n = 25) or 1.34 g biomass (±1.15 SD, range
0.15–4.72, n = 25) per 0.75 m2 in the 0–8 cm soil layer.
For only eight plots was it possible to determine earthworm
densities 8 days later. We were unable to monitor two of
the original swarm areas due to the presence of elephants;
in another nine cases we noted signs of new swarm raids
directly on or within a 10 m distance of the examined plots
and conservatively excluded all these cases. The remaining
six areas could not be re-examined due to logistical constraints or because the fieldwork ended before the 8-day
period was over. The numbers of earthworm pieces in the
plots ahead of raids were higher than those in plots
examined directly after swarm raids (paired t test, t = 2.73,
df = 24, p = 0.01), but did not differ from those measured
8 days later (paired t test, t = 1.29, df = 7, p = 0.24).
Earthworm biomass in the plots ahead of raids was neither
different from that in plots examined immediately after
swarm raids (paired t test, t = 1.63, df = 24, p = 0.12) nor
that measured 8 days later (paired t test, t = -0.53,
df = 7, p = 0.61). The largest complete earthworm specimen had a biomass of 0.922 g, 307-times the biomass of
the smallest specimen (0.003 g).
Independent estimation of swarm raid impact
based on prey composition and prey retrieval data
Among the 20 prey samples examined, Annelida made up,
on average, 50.08% (±22.40% SD) of prey biomass. This
proportion is not significantly different from the 55.16%
(±32.37% SD) obtained for the dry season months of
77
February and March in previous years at the same site by
Schöning et al. (2008) (t test, t = -0.49, df = 27,
p = 0.63). The mean prey item biomass was 2.02 mg
(8994.74 mg/4,443 items). The observed prey retrieval
rates ranged from 90 to 686 items (mean 374.75 ± 183.89
SD, n = 15) per 10 min which translates into a mean prey
retrieval rate of earthworm prey biomass of 379.10 mg per
10 min. During a 10-min period, a colony retrieves prey
from an area of 12.72 m2 (10.6 m swarm raid width 9
7.2 m/h swarm raid speed = 12.72 m2 per 10 min). Such
an area will hold on average 22.72 g earthworm prey
biomass so that the ants extract about 1.7% of the available
earthworm prey. We estimated the birds’ food intake rates
based on the assumption that they consume similar food
amounts as neotropical ant-following birds (Franks, 1980,
p. 81). If A. poliocephala birds (mass of adults about
26.55 g, Keith et al., 1992) obtain all their food at swarm
raids and rely solely on earthworms for food, the average
daily intake of 1.4 individuals (average number of birds
present at swarm raids) would equal about 17.47 g earthworm prey biomass. If these 1.4 birds forage at swarms
from dawn to dusk (13 h), they would extract an average of
0.22 g earthworm biomass per 10 min. The combined
effect of driver ant and bird predation on earthworms
would then amount to about 2.6% of the earthworm biomass in and above the 0–8 cm soil layer. In areas raided at
night, extraction rates would be correspondingly lower.
The average proportion of biomass extracted by raids over
a 24 h period is then ca. 2.2%.
Identity of available and hunted earthworms
No earthworms were found in the leaf-litter. Among the
samples of earthworms available in the 0–8 cm layer, four
species were identified (Table 2): Dichogaster (Diplothecodrilus) bolaui (length of adults 25–35 mm, diameter
1.0–1.5 mm), Di. (Diplothecodrilus) affinis (length 30–
35 mm, diameter 2.0–2.5 mm, Polytoreutus huebneri
(length 210–390 mm, diameter 5–7 mm), and P. annulatus
(length 60–65 mm, diameter 3–4 mm). The same species
except for Di. bolaui were found in the 8–30 cm layer. The
proportion of Polytoreutus individuals in the two layers
was different from that of Dichogaster species (Fisher’s
exact test, two-tailed, p = 0.001), with Polytoreutus individuals distributed more evenly between the two layers.
The two Dichogaster species are known to live in the
topmost soil layer (and are categorized as epigaeic
or endogaeic polyhumic; Hendrix and Bohlen, 2002).
P. huebneri seems to belong to the anaecic functional type
(living in permanent burrows in the soil sometimes quite
deep but feeds and defecates on the surface so they regularly come up to the surface), while the soil stratum use by
P. annulatus might be epi- to endogaeic.
78
Table 1 Earthworm prey density
before, immediately after and
8 days after swarm raids
C. Schöning et al.
Swarm raid
1
A
Swarm raid
width (m)
8.2
Number
of birds
Earthworm prey density
Before
Immediately
after
Eight days
later
3
38
11
24
0.991
0.241
1.267
17
2
C
14.6
0
27
1.886
2.255
3
A
12.2
2
70
50
1.089
0.730
4
D
7.0
2
56
13
1.588
0.203
5
C
5.0
0
8
11
17
0.327
0.284
0.655
12
16
14
0.519
0.533
0.838
36
6
The upper figure indicates the
total number of earthworm items
found in the three 50 9 50 cm2
plots, while the lower figure
represents the earthworm biomass
density (g per m2)
Colony
D
9.7
1
7
B
11.1
2
60
1.699
1.275
8
A
14.4
2
27
27
0.525
0.389
9
A
17.4
3
43
60
0.654
0.878
10
E
12.3
0
42
11
0.830
0.216
11
C
11.2
1
27
19
1.945
1.105
2.008
12
B
10.9
4
52
60
49
3.474
2.664
3.485
13
B
6.2
2
47
34
3.574
2.295
14
C
6.3
2
27
38
0.318
1.367
15
D
13.0
2
28
2
0.500
0.044
16
C
5.0
0
7
23
0.210
1.761
17
D
16.8
2
75
59
4.723
1.412
1.596
23
44
30
34
18
E
8.4
0
44
1.398
0.728
2.606
19
A
8.8
2
49
29
35
0.778
0.607
0.673
20
B
9.4
1
39
38
2.037
2.309
21
E
15.4
0
7
13
0.151
0.527
22
B
11.2
2
19
25
1.759
1.542
23
E
13.6
1
31
17
0.739
0.250
24
E
8.9
1
27
14
1.341
0.342
25
D
8.1
0
11
12
0.542
0.849
Impact of driver ant swarm raids on earthworms
79
Table 2 Identity, abundance and wet mass of available earthworms
sampled in February 2008 (40 plots each measuring 50 9 50 cm2)
Species
Number of
specimens
Wet
mass (g)
0–8 cm layer
Dichogaster bolaui
3
0.18
Di. affinis
Dichogaster spp. juv.
21
26
2.07
1.20
Polytoreutus huebneri
10
14.04
P. huebneri fragment ? juv.
0
15.39
Polytoreutus spp. fragment ? juv.
0
7.38
28
4.98
88
45.24
P. annulatus
Sum
8–30 cm layer
Di. affinis
3
0.22
19
32.63
P. huebneri fragment ? juv.
0
22.10
Polytoreutus spp. fragment ? juv.
0
5.10
P. huebneri
P. annulatus
Sum
2
0.43
24
60.48
any other afrotropical and neotropical swarm-raiding army
ant species. E. burchellii densities range between 3.5
(Barro Colorado Island/Panama; Franks, 1982) and 11
colonies per 100 ha (Corcovado/Costa Rica; Swartz, 1997),
whereas Leroux (1982) and Raignier and van Boven (1955)
reported a density of 25 colonies per 100 ha for D. nigricans in Ivory Coast and for D. wilverthi in DR Congo,
respectively. At a site in central Kenya up to four
D. molestus colonies were found nesting within a 5-ha
farmland area (80 colonies per 100 ha) for brief periods
(Gotwald, 1995), a density that may also be reached on a
similarly small-scale and for short periods at our Mount
Kenya study site. The distribution of D. molestus colonies
clearly deviates from complete spatial randomness at a
variety of spatial scales r = 30, 40, 50, 90, 100, 140, 150,
160 and 170 m (Fig. 2). The number of neighbouring
colonies found in circles of these radii centred on active
nests is lower than that expected by a random spatial distribution, indicating a ‘‘repellent’’ effect of colonies on
neighbours.
Juv. juvenile
Spatial and temporal raid patterns
Among the complete individuals in the 0–8 cm layer,
47.4% had a regenerated tail, indicating a high predation
pressure. In the 8–30 cm layer the proportion of individuals
with a regenerated tail was lower (28.6%). Earthworm
specimens with regenerated tail are easy to recognize
because the regenerated tail-part is of paler colour and its
segments are thinner.
The two Polytoreutus species constitute about 96% of
the entire earthworm biomass in the 0–30 cm layer. The
earthworms in the 8–30 cm layer represented 57% of the
total earthworm biomass available down to a depth of
30 cm.
Among the 29 earthworms taken from D. molestus
workers in swarm raids, 25 belonged to P. huebneri, three
juveniles belonged to Polytoreutus but could not be identified to species level, and one specimen was identified as
Di. affinis. The proportion of Polytoreutus individuals
among the sample of captured earthworms was thus much
higher than expected based on their relative occurrence in
the 0–8 cm layer or the entire 0–30 cm layer (Fisher’s
exact tests, in both cases p \ 0.01).
Some traps were removed by unknown animals and predation frequencies were corrected for lost trap-days. The
mean overall raid frequency was 1.61%, meaning that a
given spot was visited by army ants once every 62 days.
Predation events were concentrated in a few small areas
(Fig. 3), all of which were in the vicinity of active nests.
Raid frequencies recorded at individual traps accordingly
ranged from 0 to 24%, with 80% of all traps not containing
any army ants over the 25-day period. The raid frequency
differed significantly between transects (Kruskal–Wallis
test, H3,100 = 8.23, p = 0.042). The mean number of
Colony density and distribution
The area size determined based on GPS data was 62.35 ha,
whereas the area value found in the other map based on
bearing and distance data was 61.56 ha. Thirty-one colonies were found which translates into a colony density of
50 colonies per 100 ha (see Supplementary online material). This density is much higher than those reported for
Fig. 2 Univariate L-function (Ripley) for the distribution of
D. molestus colonies at study site 1 in February 2008. The upper
and lower envelopes represent the fifth highest and the fifth lowest of
the ranked values of L11(r) obtained from 99 Monte Carlo
simulations, respectively
80
Fig. 3 Raid rates at 100 pitfall traps placed along 4 transects over the
25-day period between 30 January and 23 February 2008
D. molestus ants in the 39 traps which captured ants was
198.2 (±188.5 SD, range 3–729).
Discussion
Impact of D. molestus swarm raids on earthworm prey
density
Driver ants and the associated birds jointly reduced the
number of earthworm pieces in the 0–8 cm layer significantly compared to pre-raid levels. However, no such effect
was found for the earthworm biomass. The pronounced
patchiness in prey density on the scale of several m2 and the
huge variation in the biomass of individual earthworms
probably made the detection of a significant reduction in
earthworm prey biomass in our data set difficult. The variable density of attending birds at the swarm front may have
further contributed to the variation in the degree by which
earthworm densities are reduced. Our estimates of the
impact based on prey retrieval and prey composition data
moreover indicate that the effective size of the reduction in
earthworm prey density was fairly small on average. Considering the large proportion of earthworm biomass in the
8–30 cm layer recorded in February 2008, we conclude that
the proportion of extracted prey biomass was probably even
much smaller than 2.2%. Why is the direct impact of swarm
raids so small? Although the biomass of soil-dwelling
earthworms is huge, the proportion of earthworms that the
ants perceive to be present (i.e. the proportion of earthworms that are truly accessible) may be small because most
earthworms are hidden. Moreover, hunting earthworms
requires a lot of time and effort (because of the need to dig)
which reduces capture rate. Immature stages of holometabolous herbivorous insects (mainly Lepidoptera and
Coleoptera) are, by contrast, much easier to find, pin down
and retrieve and will thus probably be harvested with higher
C. Schöning et al.
efficiency (prey biomass gained per unit foraging effort
invested) by the opportunistic D. molestus. We make the
testable prediction that the impact of swarm raids on the
populations of such other prey types is stronger so that the
proportion of earthworm prey in a colony’s diet is likely to
increase with increasing nest residence time.
Eight days after raids earthworm prey density (both in
terms of numbers and biomass) was not different from preraid levels. So swarm raids do not cause a discernible
reduction in local earthworm density, at least within the
8 days we examined, an outcome probably due to vertical
and/or horizontal migration of earthworms.
Our results suggest that D. molestus preferentially preys
on the larger Polytoreutus species. Since the long-legged
driver ant workers are less adept at moving through small
interstices in the soil than workers of subterranean Dorylus
species (Schöning et al., 2005b), the wider tunnels of large
earthworms may be a welcome opportunity to find and
attack earthworm prey that would otherwise be out of reach
for the predominantly surface-active D. molestus. If earthworms are mainly found when ants follow their tunnels, it is
conceivable that the ants sometimes hunt at greater depths
than the 8 cm down to which we measured earthworm
densities in the analysis of the direct impact of swarm raids.
Because the earthworm biomass in the 8–30 cm layer was
even greater than in the upper layer in February 2008, the
proportion of earthworm biomass extracted would in any
case be small. At present too little is known about the ants’
foraging behaviour in the soil, and so it is also possible that
small and large earthworms are dug out of the soil even
when there are no tunnels from the surface through which
the ants can proceed. We collected only those individuals
which came out of their tunnels trying to escape and were
then captured by the ants. Larger earthworms are certainly
easier to see and smaller earthworms might be less successful in surging out of the ground when attempting to
escape, so that our sampling strategy may have introduced
some bias. The fact that we found a significant reduction in
earthworm numbers but not in biomass suggests that small
species or individuals are preyed upon to a larger extent.
Predation of earthworm species inhabiting different strata
should in future be documented and quantified more reliably by using DNA barcoding (Hebert et al., 2003; Chang
et al., 2009) to identify the earthworm pieces retrieved by
ants on foraging trails to species level.
Since D. molestus colonies are known to move away
from their nearest neighbour when migrating to a new nest
site (Schöning et al., 2005a), one may hypothesize that
colony distribution should be regular and that raid rates
should be homogenous in space. The first hypothesis was
supported by our data, establishing migrations directed
away from conspecific colonies as an alternative mechanism to produce regular colony distribution patterns in ants
Impact of driver ant swarm raids on earthworms
(which in more sessile species such as harvester ants often
results from territorial behaviour and predation on founding queens and incipient colonies close to established
colonies; Hölldobler and Wilson, 1990). The second
hypothesis was not supported. The predation events we
recorded over the 25-day period were concentrated in a few
small areas. The observed heterogeneity of predation rates
is probably scale-dependent. If the sampling scheme had
been continued for several months, the predation frequency
might not have differed between transects and might also
have been more homogenous within transects.
Although the overall impact of swarm raids is apparently
small, ants can reduce earthworm prey density severely on
small scales when they capture large earthworms ([0.5 g
biomass, this amount exceeds the entire pre-raid biomass
found in some of the 0.75 m2 plot sets). The spatial pattern
of swarm raids may therefore contribute significantly to the
pronounced small-scale variation in earthworm density.
In spite of the apparently marginal and ephemeral
reduction of earthworm densities by swarm raids and the
relatively low raid frequency (on average once every
2 months) it is still possible that D. molestus and the
associated bird species limit earthworm populations. Driver
ant swarm raids kill and injure earthworms and influence
movement patterns and may thus have a significant impact
on earthworm reproduction. Indeed the proportion of
earthworms with regenerated tail was very high, though it
remains unclear how much other predators (such as
mammals or subterranean Dorylus species) contribute to
the high predation pressure. Caution is therefore warranted
in interpreting the results of this short-term study. A longterm exclusion experiment would be useful to clarify
whether predation by driver ants and associated birds limits
earthworm populations. Ideally, the population densities of
the four prey species will then be examined separately.
81
cigera (Freitas, 1994), on the one hand, and the swarmraiding myrmicine species Pheidologeton diversus which
feeds also to a large extent on plant-derived food types and
migrates only very rarely, on the other (Moffett, 1988). The
new findings on D. molestus in the Mount Kenya forest also
fit in well with these considerations. Superabundant detritivores (earthworms) represent a major fraction of the species’
diet so that it operates at a low trophic level and has a huge
prey base. As a consequence colony biomass density is
extraordinarily high compared to that of E. burchellii
(assuming a similar colony biomass of D. molestus and
E. burchellii). The estimated impact of D. molestus raids on
the populations of its main prey type was small and these
prey recovered quickly after raids. Colonies raiding through
an area visited 8 days earlier encounter densities of this prey
type that are on average as high as pre-raid densities. The
costs of re-using areas recently raided are therefore much
smaller than for E. burchellii colonies. And indeed, there
is considerable overlap between pre- and post-migration
foraging areas (Gotwald, 1995, Schöning et al., 2005a).
Overall, a strategy involving low migration frequency and
short migration distance is thus selectively favoured in
D. molestus.
Acknowledgments We are grateful to Washington Njagi and
Mwenda Tiraka for help during fieldwork and the Kenya Wildlife
Service and the Kenyan Ministry of Education, Science and Technology for granting research permission. We thank Klaus Riech for
preparing Fig. 1. C.S. wishes to thank Jacobus Boomsma and Eduard
Linsenmair for fruitful discussions on the impact of driver ant predation on prey populations. Jon Fjeldså confirmed the ID of Alethe
poliocephala based on pictures, and Titus Imboma kindly provided
information on ecology of this bird. Two anonymous referees made
useful suggestions that helped improve the manuscript. Financial
support was provided by the Alexander von Humboldt-Foundation
and the Danish National Research Foundation.
Prey population dynamics and D. molestus migration
behaviour
References
The implications of prey characteristics for the evolution of
optimal migration behaviour in predatory ants have been
evaluated by Gotwald (1978), Franks et al. (1999) and
Franks (2001). Comparing the prey spectra of the neotropical E. burchellii which feeds largely on the brood of
social insects (ants and wasps) and the afrotropical
D. wilverthi which feeds mostly on the immature stages of
herbivorous insects, Franks (2001) argued that species
preying on animals whose populations recover more slowly
following a raid have to migrate both more frequently
and further to avoid encountering areas from which prey
has recently been harvested. This scenario is further supported by extending the comparison to include the extremely
specialized and frequently migrating Leptogenys propefal-
Besag J. 1977. Contribution to the discussion of Dr. Ripley’s paper.
J. R. Stat. Soc. B 39: 193-195
Brussaard L. 1998. Soil fauna, guilds, functional groups and
ecosystem processes. Appl. Soil Ecol. 9: 123-135
Bussmann R. 1994. The Forests of Mt Kenya – Vegetation, Ecology,
Destruction and Management of a Tropical Mountain Forest
Ecosystem. PhD thesis, University of Bayreuth, Germany.
Chang C.-H., Rougerie R. and Chen J.-H. 2009. Identifying earthworms through DNA barcodes: pitfalls and promise.
Pedobiologia 52: 171-180
Dejean A., Schatz B., Orivel J. and Beugnon G. 1999. Prey capture
behavior of Psalidomyrmex procerus (Formicidae: Ponerinae), a
specialist predator of earthworms (Annelida). Sociobiology 34:
545-554
Dunham A.E. 2008. Above and below ground impacts of terrestrial
mammals and birds in a tropical forest. Oikos 117: 571-579
Fragoso C. and Lavelle P. 1992. Earthworm communities of tropical
rain forests. Soil Biol. Biochem. 24: 1397-1408
82
Frank D.A. 2008. Evidence for top predator control of a grazing
ecosystem. Oikos 117: 1718-1724
Franks N.R. 1980. The Evolutionary Ecology of the Army Ant Eciton
burchelli on Barro Colorado Island, Panama. PhD thesis,
University of Leeds, UK
Franks N.R. 1982. A new method for censusing animal populations:
the number of Eciton burchelli army ant colonies on Barro
Colorado Island, Panama. Oecologia 52: 266-268
Franks N.R. 2001. Evolution of mass transit systems in ants: a tale of
two societies. In: Insect Movement: Mechanisms and Consequences (Woiwod I., Reynolds D.R. and Thomas C.D., Eds).
CAB International Publishing, Wallingford, UK, pp 281-298
Franks N.R. and Fletcher C.R. 1983. Spatial patterns in army ant
foraging and migration. Eciton burchelli on Barro Colorado,
Panama. Behav. Ecol. Sociobiol. 12: 261-270
Franks N.R., Sendova-Franks A.B., Simmons J. and Mogie M. 1999.
Convergent evolution, superefficient teams and tempo in Old and
New World army ants. Proc. R. Soc. London B 266: 1697-1701
Freitas A.V.L. 1994. Nest relocation and prey specialization in the ant
Leptogenys propefalcigera Roger (Formicidae: Ponerinae) in an
urban area in southeastern Brazil. Insect. Soc. 42: 453-456
Gotwald W.H. Jr. 1974. Predatory behavior and food preferences of
driver ants in selected African habitats. Ann. Entomol. Soc. Am.
67: 877–886
Gotwald W. H. Jr. 1978. Trophic ecology and adaptation in tropical Old
World ants of the subfamily Dorylinae. Biotropica 10: 161-169.
Gotwald W.H. Jr 1995 Army Ants – The Biology of Social Predation.
Cornell University Press. Ithaca and London. 302 pp
Hebert P.D.N., Cywinska A., Ball S.L. and deWaard J.R. 2003
Biological identification through DNA barcodes. Proc. R. Soc.
London B 270: 313–321
Hendrix P.F. and Bohlen P.J. 2002. Exotic earthworm invasions in
North America: ecological and policy implications. BioScience
52: 1-11
Hölldobler B. and Wilson E.O. 1990. The Ants. Cambridge, Massachusetts: Belknap Press of Harvard University Press. 732 pp
Hooper D.U., Bignell D.E., Brown V.K., Brussaard L., Dangerfield
J.M., Wall D.H., Wardle D.A., Coleman D.C., Giller K.E.,
Lavelle P., van der Putten W.H., de Ruiter P.C., Rusek J., Silver
W.E., Tiedje J.M. and Wolters V. 2000. Interactions between
aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. BioScience 50:
1049-1061
Keith S., Urban E.K. and Fry C.H. 1992. The Birds of Africa. Vol. 4.
Academic Press. London. pp
Kingdon J. 1997. The Kingdon Field Guide to African Mammals.
Academic Press. San Diego. 450 pp
Kronauer D.J.C., Schöning C. and Boomsma J.J. 2006. Male parentage
in army ants. Mol. Ecol. 15: 1147-1151
Kronauer D.J.C., Schöning C., Vilhelmsen L. and Boomsma J.J.
2007. A molecular phylogeny of Dorylus army ants provides
evidence for multiple evolutionary transitions in foraging niche.
BMC Evol. Biol. 7: 56. http://www.biomedcentral.com/14712148/7/56
Lavelle P. 1997. Faunal activities and soil processes: adaptive
strategies that determine ecosystem function. Adv. Ecol. Res. 27:
93-132
Lavelle P., Bignell D., Lepage M., Wolters V., Roger P., Ineson P.,
Heal O.W. and Dhillion S. 1997. Soil function in a changing
world: the role of invertebrate ecosystem engineers. Eur. J. Soil
Biol. 33: 159-193
Leroux J.M. 1982. Ecologie des populations de dorylines Anomma
nigricans dans la Région de Lamto (Côte d’Ivoire). Publ. Lab.
Zool. 22. E.N.S. Paris.
C. Schöning et al.
Moffett M.W. 1988. Nesting, emigrations, and colony foundation in
two group-hunting Myrmicine ants (Hymenoptera: Formicidae:
Pheidologeton). In: Advances in Myrmecology (Trager J.C., Ed).
Leiden: E.J. Brill, pp 355-370
Perreault J.M., Whalen J.K. 2006. Earthworm burrowing in laboratory
microcosms as influenced by soil temperature and moisture.
Pedobiologia 50: 397-403
Peters M.K., Likare S., Kraemer M. 2008. Effects of habitat
fragmentation and degradation on flocks of African ant-following birds. Ecol. Appl. 18: 847-858
Raignier A., van Boven J.K.A. 1955. Etude taxonomique, biologique
et biométrique des Dorylus du sous-genre Anomma (Hymenoptera: Formicidae). Ann. Mus. R. Congo Belg. Tervuren. Sc.
Zool. 2: 1-359
Ripley B.D. 1976. The second-order analysis of stationary point
processes. J. Appl. Prob. 13: 255-266
Savage T.S. 1847. The driver ants of West Africa. Proc. Acad. Nat.
Sci. Phil. 4: 195-200
Schoener T.W. and Spiller D.A. 1996. Devastation of prey diversity
by experimentally introduced predators in the field. Nature 381:
691-694
Schöning C., Njagi W. and Franks N.R. 2005a. Temporal and spatial
patterns in the emigrations of the army ant Dorylus (Anomma)
molestus in the montane forest of Mt Kenya. Ecol. Entomol. 30:
532-540
Schöning C., Kinuthia W. and Franks N.R. 2005b. Evolution of
allometries in the worker caste of Dorylus army ants. Oikos 110:
231-240
Schöning C., Njagi W. and Kinuthia W. 2008. Prey spectra of two
swarm-raiding army ant species in East Africa. J. Zool. 274: 85-93
Schmitz O.J. 2003. Top predator control of plant biodiversity and
productivity in an old-field ecosystem. Ecol. Lett. 6: 156–163
Sih A., Crowley P., McPeek M., Petranka J. and Strohmeier K. 1985.
Predation, competition, and prey communities: a review of field
experiments. Ann. Rev. Ecol. Syst. 16: 269–312
Sims R.W. 1982. Revision of the eastern African earthworm genus
Polytoreutus (Eudrilidae: Oligochaeta). Bull. Brit. Mus. (Nat.
Hist.) Zool. Ser. 43: 253-298
Sinclair A.E. 2003. Mammal population regulation, keystone processes and ecosystem dynamics. Phil. Trans. R. Soc. Lond. B
358: 1729-1740
Sokal R.S. and Rohlf F.J. 1995. Biometry. 3rd Ed. W.H. Freeman,
New York. 887 pp
Speck H. 1983. Mount Kenya Area. Ecological and Agricultural
Significance of the Soils. Geographica Bernensia. African
Studies A2
Stevenson T. and Fanshawe J. 2002. Field Guide to the Birds of East
Africa. T. and A.D. Poyser. 600 pp
Swartz M.B. 1997. Behavioral and Population Ecology of the Army
Ant Eciton burchelli and Ant-Following Birds. PhD thesis.
University of Texas, Austin, USA
Terborgh J., Lopez L., Nuňez P., Rao M., Shahabuddin G., Orihuela
G., Riveros M., Ascanio R., Adler G.H., Lambert T.D. and
Balbas L. 2001. Ecological meltdown in predator-free forest
fragments. Science 294: 1923-1926
Vosseler J. 1905. Die ostafrikanische Treiberameise (Siafu). Der
Pflanzer 1: 289-302
Weber N.A. 1943. The ants of the Imatong Mountains, AngloEgyptian Sudan. Bull. Mus. Comp. Zool. Harvard Coll. 93: 263389
Wiegand T. and Moloney K.A. 2004. Rings, circles, and null-models
for point pattern analysis in ecology. Oikos 104: 209-229
Wilson E.O. 1958. The beginnings of nomadic and group predatory
behaviour in the ponerine ants. Evolution 12: 24-36