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Opportunist slave-making ants Myrmoxenus ravouxi discriminate different host species from a non-host species

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Slave-making ants exploit the worker force of host colonies permanently and have to make recurrent raids in order to replenish the slave’s stock. Some of these parasite species exploit different host species and few studies so far have been devoted to host species recognition mechanisms. Here, we tried to determine if opportunist slave-making ants using different host species rely on innate or experience-induced preferences to discriminate host from non-host species. We show that Myrmoxenus ravouxi slave-making workers are not only more aggressive toward heterocolonial host and potential host species workers when compared with non-host species workers, but also toward heterocolonial host workers than toward heterocolonial conspecifics. Moreover, M. ravouxi workers display more antennations and contacts toward the heterocolonial host species when compared with the non-host species. We also show that they do not discriminate between homocolonial and heterocolonial conspecifics. Together, our results suggest that this opportunistic slave-making ant species may have a complex social recognition template based on both innate and experience-based mechanisms.
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RESEARCH ARTICLE
Opportunist slave-making ants Myrmoxenus ravouxi discriminate
different host species from a non-host species
O. Delattre
N. Cha
ˆ
line
S. Chameron
E. Lecoutey
P. Jaisson
Received: 9 May 2012 / Revised: 24 August 2012 / Accepted: 25 August 2012 / Published online: 12 October 2012
Ó International Union for the Study of Social Insects (IUSSI) 2012
Abstract Slave-making ants exploit the worker force of
host colonies permanently and have to make recurrent raids
in order to replenish the slave’s stock. Some of these parasite
species exploit different host species and few studies so far
have been devoted to host species recognition mechanisms.
Here, we tried to determine if opportunist slave-making ants
using different host species rely on innate or experience-
induced preferences to discriminate host from non-host
species. We show that Myrmoxenus ravouxi slave-making
workers are not only more aggressive toward heterocolonial
host and potential host species workers when compared with
non-host species workers, but also toward heterocolonial
host workers than toward heterocolonial conspecifics.
Moreover, M. ravouxi workers display more antennations
and contacts toward the heterocolonial host species when
compared with the non-host species. We also show that they
do not discriminate between homocolonial and heteroco-
lonial conspecifics. Together, our results suggest that this
opportunistic slave-making ant species may have a complex
social recognition template based on both innate and expe-
rience-based mechanisms.
Keywords Social parasitism Slave-making ants
Social recognition Temnothorax Coevolution
Introduction
Slave-making ants invade and periodically raid neighboring
colonies of their host species to pillage their brood (Bus-
chinger, 1986, 2009), creating ‘chimeric’ societies of two
or more species. With a lifespan of sometimes more than
10 years, these colonies may comprise individuals from
different colonies and/or species with no overt conflict. The
slave brood is brought back from raided host colonies, fol-
lowing a typical behavioral sequence (Buschinger et al.,
1980).
For example, in the slave-making ant Myrmoxenus rav-
ouxi, around the end of spring, parasite workers prospect
around the nest until they find a host colony. Then, when a
scout is successful, it returns to its nest and stimulates her
parasite nestmates. This ‘group recruitment’’ will launch the
raid itself (Winter, 1979). After almost all defenders have fled
or have been killed by the parasite workers, the members of
the parasite colony (both parasites and slaves) take the
brood and bring it back to their nest, where it will emerge.
M. ravouxi is an opportunistic slave-maker parasitizing more
than five Temnothorax species (Buschinger and Winter,
1983;Buschinger,1989, 1997; Seifert, 2007). Such a strategy
could represent an adaptive advantage for the parasite, thus
accounting for the wider repartition area of M. ravouxi within
its genus (Buschinger, 1997; Seifert, 2007). Yet, it is still
crucial for a slave-making worker to recognize its different
host from the non-host species during raids. Indeed, workers
from non-host species, more distant phylogenetically
(Emery, 1909; Beibl et al., 2005), may not be suitable nurses
for the parasite brood. This could increase the mortality rate
and impact the parasitized colonies’ fitness. Moreover, non-
host defenses may be more difficult to overcome for parasite
workers, as social parasites often exhibit specific adaptations
to their host species (Lenoir et al., 2001; Foitzik et al., 2001,
O. Delattre (&) N. Cha
ˆ
line S. Chameron E. Lecoutey
P. Jaisson
Laboratoire d’Ethologie Expe
´
rimentale et Compare
´
e,
EA 4443, Universite
´
Paris 13, 99 avenue Jean-Baptiste Cle
´
ment,
93430 Villetaneuse, France
e-mail: olivier.delattre@leec.univ-paris13.fr
Insect. Soc. (2013) 60:7–13
DOI 10.1007/s00040-012-0257-3
Insectes Sociaux
123
2003; Brandt and Foitzik, 2004). Therefore, discrimination
abilities in parasite species between potential hosts and other
species are likely to evolve to be more efficient to discrimi-
nate suitable host species.
Members of a colony use a neural template of a common
colonial label, which is learned as early as the pre-imaginal
development phase in ants (Isingrini et al., 1985), to dis-
criminate nestmates from aliens (Lenoir et al., 1999). Inside
the colony, individual chemical cues are blended together in
the common label via allogrooming, passive contacts and
trophallaxis (Soroker et al., 1994, 2003). This mechanism has
been termed the ‘Gestalt’’ model by Crozier and Dix (1979).
Experiments with artificial mixed-species colonies of
ants have shown that workers were less agressive toward
non-nestmates when their colonial odor was more complex
(Errard, 1994; Errard et al., 2006). This has been attributed
to the fact that a richer colonial label leads ants to form a
broader recognition template that increases their tolerance
threshold, leading to more frequent acceptation errors
(Reeve, 1989; Errard et al., 2006). Slave workers raise and
feed parasite brood until their emergence and forage for the
entire colony, while slave-making workers are most of the
time inactive inside the nest (Buschinger, 1986). Emerging
parasite workers may thus learn the colonial label essen-
tially from the interactions with their slave workers. They
may develop also a larger colonial template which reduces
their ability to discriminate their host from their own species
(Errard, 1994; Errard et al., 2006).
Myrmoxenus ravouxi often lives in areas where different
host species are present. Nonetheless, parasitized colonies
with more than one enslaved species are rare and we do not
know if this is because the pillaged brood from a different
host species is destroyed by slaves or if parasite workers
exclusively raid neighboring colonies of the imprinted host
species. Indeed, we know that the species of the actual slave
workers may influence slave-maker workers behavior, since
expressed preferences for a more common host in a popu-
lation may yield to adaptive plasticity, particularly during
raids (Schumann and Buschinger, 1995). Nonetheless, the
authors of this study also demonstrated that workers from
the slave-making ant Chalepoxenus muellerianus, enslaving
two different host species, displayed an innate preference
toward their main host species, irrespective of the species
they were reared with.
In this experiment, we chose to test if a highly opportunist
slave-making parasite was able to discriminate between non-
host, potential host, host and parasite workers (homo or
heterocolonial for the last two) to assess if these social
parasites rely on innate or experience-induced preferences
to discriminate their host species and raid neighboring
colonies.
We studied whether M. ravouxi could discriminate (1)
between a familiar (actual) and non-familiar host species
and (2) between a potential (unfamiliar) host species and a
non-host species. We monitored slave-making workers’
aggressiveness and affiliative behaviors, such as antenna-
tions and contacts, to test for host species discrimination
when different social stimuli were presented. We also tested
whether M. ravouxi workers exhibited a different behavior
toward their own species. Indeed, the Gestalt model predicts
that the colonial odor will be homogenized in a mixed-
species colony, making species discrimination difficult
(Errard, 1994; Errard and Hefetz, 1997; Errard et al., 2006).
However, the behavioral repertoire and the role of slaves
and slave makers in parasitized colonies are very different
(Buschinger and Winter, 1983; Buschinger, 1986) and
species recognition in this context could allow better pro-
ductivity of parasitized colonies, which could for example
increase raid efficiency.
Methods
Species
We chose M. ravouxi as our focal species. This species is a
slave-making social parasite with a wide distribution in
Europe ranging from France to Greece (Buschinger, 1997).
It is known to parasitize several species of the diversified
genus Temnothorax (Buschinger and Winter, 1983,Busch-
inger, 1989, Buschinger, 1997), among which are Temno-
thorax unifasciatus and T. rabaudi. We used the main host
(T. unifasciatus) and a potential host species (T. rabaudi)
from an M. ravouxi parasitized population to assess if the
social parasite was able to discriminate between its host, a
potential host and a non-host species (T. nylanderi).
We collected the parasite (N = 12), parasite-free host
(N = 14), potential host (N = 9) and non-host (N = 7) col-
onies in Vaison-la-Romaine (44°14
0
N, 5°04
0
E) in August
2006. Colonies were reared at the laboratory in small plastic
boxes (15 9 10 9 5 cm) with a plaster soil as foraging area,
in a nest made from two microscope slides superimposed
with a 1-mm free space between them. All colonies were fed
once a week with honey and fruit flies. The experiments took
place in the late spring, from May to June 2007, after a
3-month wintering period at 8 °C from December to March.
The photoperiod was 12/12 h with a night temperature of
15 °C and a day temperature of 22 °C at the time of the
experiment. The humidity was kept around 60 %.
Experimental design
We used dyadic presentations to test the discrimination
abilities of M. ravouxi workers. These comparisons could
be categorized in ‘nestmates versus non-nestmates’ and
‘host versus non-host’ recognition tasks (Table 1).
8 O. Delattre et al.
123
Our experimental device was a circular arena (3 cm
diameter) where two workers (used as stimuli) were tied at
opposite sides with a thin nylon filament between their head
and thorax. To limit moves and reciprocal interactions,
these workers were also anesthetized beforehand with car-
bon dioxide for 15 s. Then, we introduced a slave-making
worker in the arena and covered the device with a thin glass
slide. No ant was used for more than one test, as experi-
mental focus or as social stimuli.
Behavioral observations
Our tests lasted for 10 min. We recorded mean antennation
and close-contact durations, which we assume are repre-
sentative, respectively, of the interest for the congener and
affiliative behaviors. The intensity of the agonistic response
of M. ravouxi workers during the tests was assessed using
the mean duration of bites. Stinging was also observed but
less often than bites, maybe because parasite workers
preferentially display this behavior during raids. We dis-
carded the tests were no contact occurred within 2 min.
Comparisons were performed using permutation tests for
paired samples. All statistical tests were implemented with
StatXact (Cytel Studio, version 8.0.0, 2007).
Results
Antennations
Myrmoxenus ravouxi workers antennated heterocolonial
workers from the host species T. unifasciatus longer than
workers from the non-host species T. nylanderi (Fig. 1;
Permutation test; t =-2.848, P = 4.8.10
-4
). Other com-
parisons were not statistically different (P [ 0.368).
Contacts
Myrmoxenus ravouxi workers stayed more in contact with
their parasite sisters than with their slaves (Fig. 2; Permu-
tation test; t = 2.384, P = 0.0134). They also remained for
more time in contact with heterocolonial free-living host
workers from the host species T. unifasciatus than with
workers from the non-host species T. nylanderi (t =
-2.169, P = 9.8.10
-4
). Other comparisons were not sig-
nificant (P [ 0.127).
Bites
Myrmoxenus ravouxi workers were more aggressive toward
T. unifasciatus heterocolonial host workers than toward
M. ravouxi heterocolonial parasite workers (Fig. 3; per-
mutation test; t =-1.831, P = 0.0312). They also bit more
T. unifasciatus heterocolonial host workers than T. nylan-
deri non-host workers (t =-1.96, P = 0.0156). Finally,
they aggressed more workers from the potential host spe-
cies T. rabaudi than workers from the non-host species
T. nylanderi (t =-2.198, P = 9.8.10
-3
). Other comparisons
were not statistically different (P [ 0.125).
Table 1 Main results with sample sizes and significance degrees
N Antennation Contact Biting
Nestmates versus non-nestmates Homocolonial parasite versus heterocolonial parasite 20 NS NS NS
Homocolonial parasite versus homocolonial slave 15 NS * NS
Heterocolonial parasite versus heterocolonial slave 18 NS NS *
Host versus non-host Potential host versus unparasitized host 13 NS NS NS
Non-host versus unparasitized host 13 *** *** *
Non-host versus potential host 20 NS NS **
NS non-significant, * P \ 0.05; ** P \ 0.01; *** P \ 0.001
Fig. 1 Mean duration of antennation in seconds (±SE) of M. ravouxi
workers during test choices with homocolonial and heterocolonial M.
ravouxi parasites (Homoc. parasite and Heteroc. parasite), homocolo-
nial and heterocolonial T. unifasciatus slaves (Homoc. and Heteroc.
slaves), unparasitized T. unifasciatus hosts (Unpar. host), potential T.
rabaudi hosts (Pot. host) and T. nylanderi non-hosts (Non-host).
***P \ 0.001
Myrmoxenus ravouxi discriminates host species from non-host species 9
123
Table 1 summarizes our different results.
Discussion
In heterospecific encounters, slave-making workers dis-
played more aggressive behaviors against workers from host
and potential host species than against non-host workers.
Moreover, parasite workers did not bite more workers from
the host than from the potential host species. Taken together,
these results suggest that M. ravouxi workers discriminate
host species from non-host species, but not their host species
from a potential host species. Our colonies were kept
isolated in the laboratory from autumn to spring, so that
no familiarization effect to any species could affect the
behavioral response of our workers during the tests (Heinze
et al., 1996; Knaden and Wehner, 2003; Sanada-Morimura
et al., 2003). Therefore, M. ravouxi workers’ discrimination
between host—familiar or not—and non-host species is at
least partially independent of previous experience.
Because slave-making ants depend on their host species
during the entire colony’s life, raids are necessary to
replenish the worker force as the slave stock decreases with
time. Thus, the selection pressure is strong on parasite
societies to be able to find and pillage host colonies and to
discriminate suitable host from non-host species (Foitzik
et al., 2001, 2003; Hare and Alloway, 2001; Blatrix and
Herbers, 2003; Brandt and Foitzik, 2004; Fischer and
Foitzik, 2004; Brandt et al., 2005; Fischer-Blass et al.,
2006). Therefore, a genetically based recognition template
of potential hosts appears all the more adaptive than it can
allow host shifting or raiding on different species according
to the most commonly available host species. Indeed,
M. ravouxi exploits at least six different hosts (Buschinger,
1989; Seifert, 2007). Phylogenetic data suggest that these
host species are closely related to each other, and that the
Myrmoxenus genus has already a long independent evolu-
tionary history from the Temnothorax genus (Beibl et al.,
2005). We can thus hypothesize that this slave-making
species derived from and/or parasitized a common ancestor
to its group of host species (Emery, 1909; Baur et al., 1995;
Parker and Rissing, 2002; Sumner et al., 2004). These
species may share some common cuticular compounds,
which may be used by the slave maker to recognize them as
potential hosts. Moreover, M. ravouxi olfactory system may
have been selected for better discrimination of host species,
as a consequence of a coevolutionary process (Thompson,
1994) between this slave-making ant and its host species.
However, the fact that we recorded no difference in aggres-
siveness of M. ravouxi workers for the host-potential host
comparisons could also be interpreted as a consequence of a
standardized environment, as we kept in isolation our colo-
nies for 6 months prior to the tests. Some studies indeed
demonstrated that diet and environment could influence the
colony odor (Crosland, 1989; Liang and Silverman, 2000;
van Zweden et al., 2009b; see Sturgis and Gordon, 2012).
Still, van Zweden et al. (2009a
) also showed that a homog-
enized environment will not affect the discrimination ability
of ants, suggesting that heritable cues play the most impor-
tant part in nestmate recognition (van Zweden et al., 2010).
Fig. 2 Mean duration of contact in seconds (±SE) during test choices
with homocolonial and heterocolonial M. ravouxi parasites (Homoc.
parasite and Heteroc. parasite), homocolonial and heterocolonial T.
unifasciatus slaves (Homoc. and Heteroc. slaves), unparasitized T.
unifasciatus hosts (Unpar. host), potential T. rabaudi hosts (Pot. host)
and T. nylanderi non-hosts (Non-host). *P \ 0.05, ***P \ 0.001
Fig. 3 Mean duration (logarithmic scale) of bites in seconds (±SE)
during test choices with homocolonial and heterocolonial M. ravouxi
parasites (Homoc. parasite and Heteroc. parasite), homocolonial and
heterocolonial T. unifasciatus slaves (Homoc. and Heteroc. slaves),
unparasitized T. unifasciatus hosts (Unpar. host), potential T. rabaudi
hosts (Pot. host) and T. nylanderi non-hosts (Non-host). *P \ 0.05,
**P \ 0.01
10 O. Delattre et al.
123
Parasite workers antennated and stayed more in contact
with their host species workers than with the non-host
workers, displaying non-agonistic and affiliative behaviors
toward them. This may be related to the fact that the recog-
nition template of M. ravouxi workers comprises some of the
familiar host species-specific chemical cues. In the study of
Schumann and Buschinger (1995), C. muellerianus workers
imprinted on the potential host label inspected potential host
species nest entrances more often than workers imprinted on
the main host species, so that an effect of experience could
not be entirely rejected. In our experiment, M. ravouxi
workers were certainly more familiar with the species-spe-
cific chemical cues of T. unifasciatus, and their recognition
template is likely to include them, at least partially. This
could explain here the more frequent affiliative behaviors
displayed toward the host species. Heterocolonial workers
from their host species may elicit affiliative or aggressive
behaviors depending on whether they are perceived under or
over the tolerance threshold of parasite workers (Reeve,
1989). Nonetheless, the experimental design used here offer
a choice between different social stimuli at the same time.
This forced the contrast between stimuli and may have
influenced the behavioral decisions because of these stressful
conditions, but gives us an interesting insight into the dis-
crimination abilities of M. ravouxi workers.
We did not record any difference in aggressiveness of
parasite workers toward their slaves and their sisters. Within
parasitized colonies, parasite and slaves are likely to share
common cuticular compounds and to display the same colo-
nial label (Franks et al., 1990;Kaibetal.,1993; Bonavita-
Cougourdan et al., 1996, 1997; d’Ettorre et al., 2002;
Brandt et al., 2005; reviewed in Lenoir et al., 2001). Ho-
mocolonial slaves are perceived as nestmates by M. ravouxi
workers (see Lenoir et al., 1999). Nonetheless, it has been
demonstrated that in experimental mixed-species colonies,
different species can keep distinct profiles (Errard et al.,
2006). Here, M. ravouxi workers displayed an affiliative
preference for their nestmate sisters, as they stayed more in
contact with them than with the slaves of their colony.
Consequently, this test clearly showed that M. ravouxi
workers discriminated their sisters from their slaves in these
experimental conditions.
Parasite workers did not behave differently toward con-
specific heterocolonial workers than toward their sisters,
but, in the presence of a parasite and a slave of another
colony, they were also more aggressive toward slaves. It
reinforces the idea that parasite workers’ discrimination
between species inside a parasitized colony could be the
consequence of them having a colonial template where
species-specific cues play a major role, thus allowing the
discrimination of host slaves, which display a slightly dif-
ferent chemical signature than the parasite workers. The
high weight of parasite species-specific cues in the matching
process between the perceived odor and the template,
combined to the permissive tolerance threshold imposed by
the mixed colony condition, could then explain the high
tolerance for homospecific congeners, be they from another
colony or not. This ability could even be beneficial, since
relying on specific cues may for instance enable M. ravouxi
workers to avoid agonistic interactions when encountering
heterocolonial homospecific workers during raiding peri-
ods. Although Schumann (1992) observed occasional
intraspecific raids in C. muellerianus in a field study, since
then very few studies have been devoted to intraspecific
slavery in slave-making ants (Le Moli et al., 1993; Kronauer
et al., 2003). Moreover, it seems difficult to disentangle the
mechanisms of such a behavior without repeated field
observations coupled with population studies. Territorial
conflicts could lead to attacks of neighboring colonies, and
the brood could then be opportunely brought back into the
nest (Wilson, 1975; Alloway, 1980
; Stuart and Alloway,
1982; Pollock and Rissing, 1989; Foitzik and Heinze, 1998;
see Buschinger, 2009). But Le Moli et al. (1993) recorded
almost no aggressive behavior between residents and
invaders in Polyergus rufescens, and pillages did not last.
This could be interpreted as an ‘error’ in the raiding
attempt, with invaders not completing the entire cycle of
their raids. Indeed, during the raiding period, one may
hypothesize that scouts could trail territorial marks of a
colony to find a suitable target (Franks et al., 2007a, b; Cao
and Dornhaus, 2012). In parasitized colonies, because for-
agers are enslaved host workers only (Buschinger, 1986),
these marks may contain species-specific host chemical cues
that could be mistakenly lead parasite workers to initiate a
raid, as observed by Schumann (1992) and Le Moli et al.
(1993), on a parasite colony. Because parasitized colonies
chemical label includes both species-specific cues of host
and parasite species, it thus support the idea that host species-
specific cues may also have a heavier relative weight either
in the perceptual component or in the decision process of
slave-making ants, which increases the efficiency of raids by
facilitating the recognition of host species.
Acknowledgments Olivier Delattre was supported by the French
Ministry of Research. Nicolas Cha
ˆ
line and Ste
´
phane Chameron were
supported by the ANR project SEUILS ANR-09-JCJC-0031.
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Myrmoxenus ravouxi discriminates host species from non-host species 13
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... M. ravouxi scouts also have no interest in engaging in fights in non-host species colonies. Slavemaking ants may discriminate host from non-host species colonies, using for example a recognition template based on innate or experience-induced preferences [50,51]. They could then also actively avoid conflicts with non-host workers by inducing ejection behaviors. ...
... We do not know how ants' decision rules are implemented , i.e. following qualitative or quantitative dissimilarity of chemical cues. Ants certainly may adjust their behavior according to the absence/presence of some particular chemical cues when facing conspecifics [51,52]. So, we think that standardization of behavioral results by chemical distance between colonies in social insects may bring new insights on the discrimination mechanisms towards sympatric species of social parasites. ...
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Full-text available
Background Social parasitism is an important selective pressure for social insect species. It is particularly the case for the hosts of dulotic (so called slave-making) ants, which pillage the brood of host colonies to increase the worker force of their own colony. Such raids can have an important impact on the fitness of the host nest. An arms race which can lead to geographic variation in host defenses is thus expected between hosts and parasites. In this study we tested whether the presence of a social parasite (the dulotic ant Myrmoxenus ravouxi) within an ant community correlated with a specific behavioral defense strategy of local host or non-host populations of Temnothorax ants. Social recognition often leads to more or less pronounced agonistic interactions between non-nestmates ants. Here, we monitored agonistic behaviors to assess whether ants discriminate social parasites from other ants. It is now well-known that ants essentially rely on cuticular hydrocarbons to discriminate nestmates from aliens. If host species have evolved a specific recognition mechanism for their parasite, we hypothesize that the differences in behavioral responses would not be fully explained simply by quantitative dissimilarity in cuticular hydrocarbon profiles, but should also involve a qualitative response due to the detection of particular compounds. We scaled the behavioral results according to the quantitative chemical distance between host and parasite colonies to test this hypothesis. Results Cuticular hydrocarbon profiles were distinct between species, but host species did not show a clearly higher aggression rate towards the parasite than toward non-parasite intruders, unless the degree of response was scaled by the chemical distance between intruders and recipient colonies. By doing so, we show that workers of the host and of a non-host species in the parasitized site displayed more agonistic behaviors (bites and ejections) towards parasite than toward non-parasite intruders. Conclusions We used two different analyses of our behavioral data (standardized with the chemical distance between colonies or not) to test our hypothesis. Standardized data show behavioral differences which could indicate qualitative and specific parasite recognition. We finally stress the importance of considering the whole set of potentially interacting species to understand the coevolution between social parasites and their hosts.
... Помимо визуальных стимулов, для распознавания различных (в том числе и потенциально опасных) объектов муравьи часто используют химические сигналы. Так, по составу кутикулярных углеводородов они легко распознают «чужих» среди своих сородичей [Lahav et al., 1999;D'Ettorre, Lenoir, 2010], а муравьи-рабовладельцы -своих потенциальных рабов [Delattre et al., 2013]. Некоторые афидофаги, в частности личинки сирфид, даже используют хемомимикрию (сходство кутикулярных углеводородов с таковыми у тлей) для предотвращения атаки муравьёв [Lohman et al., 2006]. ...
... (3) exploratory behavior: exploration of the aphidophage by the antennae; (4) aggression poses: "alert pose," an almost immobile posture with mandibles open and antennae raised and directed towards the aphidophage, and "aggression pose," a pose with abdomen bent, ready to discharge a portion of acid; (5) body jerking: quick movements toward the aphidophage with open mandibles, without actual contact; (6) hit-and-run attacks: quick movements with open mandibles, ending in contact with the aphidophage; (7) bites: bites or series of bites (< 10 s); (8) death grip: grasping the aphidophage with mandibles and legs (> 10 s), with bending of the abdomen and spraying the enemy with acid. The ant reactions were split into two groups by the degree of aggression: "nonaggressive" (1-4) and "aggressive" ones (5)(6)(7)(8). If the ant demonstrated a spectrum of reactions in rapid succession, the most aggressive reaction was used in the analysis. ...
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Honeydew collectors of Formica pratensis taken from the nature (control) and laboratory-reared “naïve” ants, which had never met either “mature” workers or aphids and aphidophages, were observed during their interactions with various aphid enemies: adults and larvae of ladybirds and lacewings, and larvae of syrphid flies. The naïve ants were significantly more aggressive towards adults than towards larvae of aphidophages. More than 70% of the naïve ants treated ladybirds and lacewings as enemies at their first encounter and attacked them immediately without any prior antennation. The frequency of aggressive reactions (body jerking and bites) towards larvae was significantly higher in the control group, whereas the percentage of ants showing explorative behavior was significantly higher in the naïve ants. Overall, experience proved to be not important for displaying the key behavioral reactions towards adult ladybirds and lacewings underlying the protection of trophobionts from these natural enemies. However, accumulation of experience is assumed to play an important role in the recognition of aphidophage larvae and formation of aggressive behavior towards them.
... The other host is T. "crasecundus", a species closely related to T. nylanderi and T. crassispinus. This is particularly surprising, as species of this taxonomic group, though abundant throughout much of the range of Myrmoxenus, are rarely if ever parasitized (Buschinger, 1989;Delattre et al., 2012Delattre et al., , 2013but see Mei, 1992). Active slave-raiding may also be the explanation for genotypes of M. tamarae workers that did not match the typical sociogenetic structure of Myrmoxenus, monogyny and monandry (a single, singly mated queen per colony). ...
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Full-text available
The ant genus Myrmoxenus consists of about ten socially parasitic species including active slave-makers and workerless "degenerate slave-makers". Myrmoxenus tamarae was previously known only from type material, two workers collected at Daba, Georgia and nothing was known about its life history, colony structure or the morphology of its sexuals. An inspection of colonies of M. tamarae near the type locality in 2010 indicates that young queens of M. tamarae invade Temnothorax nests and kill the host queen by throttling. The simultaneous presence of two slave species in a single colony (an undescribed species related to T. nylanderi and a species morphologically resembling T. unifasciatus) indicates that M. tamarae is an active slave-maker. The genetic structure of the colonies matches that expected for a monogynous and monandrous ant, but three of eight colonies inspected appeared to contain workers belonging to an additional genetic lineage.
... The other host is T. "crasecundus", a species closely related to T. nylanderi and T. crassispinus. This is particularly surprising, as species of this taxonomic group, though abundant throughout much of the range of Myrmoxenus, are rarely if ever parasitized (Buschinger, 1989;Delattre et al., 2012Delattre et al., , 2013but see Mei, 1992). Active slave-raiding may also be the explanation for genotypes of M. tamarae workers that did not match the typical sociogenetic structure of Myrmoxenus, monogyny and monandry (a single, singly mated queen per colony). ...
Article
Full-text available
The ant genus Myrmoxenus consists of about ten socially parasitic species including active slave-makers and workerless “degenerate slave-makers”. Myrmoxenus tamarae was previously known only from type material, two workers collected at Daba, Georgia and nothing was known about its life history, colony structure or the morphology of its sexuals. An inspection of colonies of M. tamarae near the type locality in 2010 indicates that young queens of M. tamarae invade Temnothorax nests and kill the host queen by throttling. The simultaneous presence of two slave species in a single colony (an undescribed species related to T. nylanderi and a species morphologically resembling T. unifasciatus) indicates that M. tamarae is an active slave-maker. The genetic structure of the colonies matches that expected for a monogynous and monandrous ant, but three of eight colonies inspected appeared to contain workers belonging to an additional genetic lineage.
Article
Slave-making ants exploit the societies of host ant species and are typically rare and patchily distributed. IUCN considers almost all slave-making ants as vulnerable, but solid data on their actual abundance are uncommon. Here we examine the genetic structure of populations of two species of the socially parasitic genus Myrmoxenus, which differ strongly in dispersal behavior and the occurrence of slave-raids. Microsatellite genotypes suggest strong differentiation even among neighboring populations of both species. FST-, G″ST-, and D-values were considerably higher in the “degenerate slave-maker” M. kraussei from Northern Italy than in the active slavemaker M. ravouxi from Southern Germany. This matches observations that sexuals of M. kraussei mate in their natal nest and queens disperse on foot while sexuals of M. ravouxi engage in mating and dispersal flights. Allelic richness was surprisingly high in both species and did not suggest recent bottlenecks, indicating that populations are larger and less vulnerable than expected from the difficulties of locating nests. Despite of considerable inbreeding, only very few diploid males were detected, supporting the view that at least in M. kraussei sex is not determined by single locus complementary sex determination unlike most other social Hymenoptera. The mismatch between the genetic and social structure of M. ravouxi colonies indicates occasionally fusion of slave-maker colonies in the field, mutual raids, or queen replacement. Complementary analyses of the host species of the two social parasites, Temnothorax unifasciatus and T. recedens, revealed low levels of population differentiation and confirmed the colony structure with a single, singly-mated queen.
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Nestmate recognition is the process by which individuals discriminate between nestmates and con- and hetero-specifics. Nestmate recognition is based on recognition cues, which include cuticular hydrocarbons (CHCs). Models of nestmate recognition predict that recognition decisions are based on the overlap of recognition cues. Colony recipients assess cue differences by comparing an individual's CHC profile to an internal template, which is based on the colony-specific cues. The behavioral response to this assessment depends on cue similarities or differences with the template. Ants show graded responses to cue differences. More recent models of nestmate recognition include adjustable thresholds that account for graded responses and intra-colony individual variation in behavioral responses towards non-nestmates. Ants display differing levels of aggression towards conspecifics under different contexts, which suggests that nestmate recognition is context-dependent. Here, we review models of decision rules and the role of CHCs in nestmate recognition. We discuss the role of ecological and social context in nestmate recognition, and explore future directions of research for the field.
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Full-text available
Colonial identity in social insects is based on nestmate recognition which is mediated through cuticular substances. Although this is considered to be distinct from kin recognition, it is possible that through evolution the signal mediating kinship was replaced by the signal mediating "nestmateship". Cuticular hydrocarbons in Cataglyphis niger are responsible for modifying the ant's aggressive behavior and are considered to have a similar function in other ants species. In ants, the postpharyngeal gland (PPG) serves as a storage organ for these cues and functions as a "gestalt" organ, with the gestalt being permanently updated. Its content is constantly being exchanged with nestmates through trophallaxis and allogrooming. We hypothesize that already in the primitive ponerine ants the PPG evolved as a gestalt organ even without trophallaxis. We discuss two alternative primary selective pressures for the evolution of trophallaxis: facilitating food exchange versus exchanging recognition cues. Callow workers seem to be characterized by a "cuticular chemical insignificance" followed by a "chemical integration" period when they acquire the gestalt of the colony and learn the associated template. We hypothesize that the template has evolved from a simple personal chemical reference in primitive species with small colonies to an internal representation of the colonial identity in larger colonies.
Article
Full-text available
Ecological constraints on the success of independent colonies are thought to strongly shape the organization of ant societies. One of the most important factors is probably the availability of suitable empty nest sites. By population censuses, laboratory experiments, and microsatellite analyses, we investigated the colony and population structure of the small, myrmicine ant Leptothorax (Myrafant) nylanderi in a deciduous forest near Wurzburg, Germany, where nest sites appear to be strongly limited, especially in late summer. Colonies of L. nylanderi inhabit cavities in rotting branches, hollow acorns, grass stems, etc. After hibernation, a temporary overabundance of empty nest sites facilitates the fragmentation of larger colonies into smaller buds, which, because the species is monogynous, are in part queenless. Nest sites become scarce in summer due to rapid decay, and both established colonies and young founding queens face a severe shortage of suitable nest sites. This leads to the fusion of established, unrelated colonies, which after initial fighting permanently merge and live together. Typically only one queen survives after fusion. Similarly, young mated queens may seek adoption in alien nests instead of founding their own colonies solitarily, and here again only a single queen survives. This temporary intraspecific parasitism may be an important first step in the evolution of obligatory permanent parasitism, which is widespread in the genus Leptothorax.
Article
The latest review of social parasitism in ants was published in 1990. Since then, comparatively few new parasitic species have been discovered, but research has progressed our knowledge of the evolution of social parasitism and the mecha-nisms involved in the maintenance of parasitic relations between species. Temporary social parasitism, slave-making, inquilinism and xenobiosis are confirmed as the primary manifestations of ant social parasitism. So-called intraspecific social parasitism should be clearly set off against the obligatory interspecific relations of social parasite and host species.A few evolutionary transitions from one of the interspecific forms to another do occur, mainly from slave-making to a derived, workerless state. Nevertheless there is no evidence for the evolution of all types of social parasitism towards inquilinism via multiple pathways as had been formerly suggested. Emery's rule sensu lato has been confirmed by mole-cular techniques. Host-parasite recognition is mediated by cuticular signatures and involves imprinting. Increasingly, social parasitic ants are considered interesting with respect to understanding conflict and cooperation among ants. Co-evolution of social parasites with the respective host species and influence of social parasites on host populations are inten-sively studied. There are still unanswered questions with respect to the unequal distribution of social parasites among the extant ant subfamilies and genera, as well as their geographic distribution including the lack of slave-makers in the tropics.
Analysis of cuticular hydrocarbon mixtures of the slave-making ant Polyergus rufescens and the Formica rufibarbis or F. cunicularia slaves with which it was living either naturally or after the slave species had been experimentally exchanged showed that cohabitation induced no qualitative homogenization of these species' cuticular signatures. The proportions of hydrocarbons common to both species tended however to be adjusted (in the case of the natural associations) or readjusted (in that of the experimental associations), especially in Polyergus towards those of their partners. On the other hand, differences were observed between the cuticular profiles of Polyergus and their Formica slaves which had been living separately from the original colony for several weeks in an experimental group, and those of the members of the original colony. The changes in the cuticular profiles occurred synchronously in all the individual members of the group. Comparisons between the cuticular versus postpharyngeal slave-maker and slave mixtures showed the existence of qualitative differences between the two mixtures. This indicates that the postpharyngeal glands are not directly involved in the production of the cuticular signatures. Some possible explanations for these results are discussed. (C) 1997 Elsevier Science Inc.
Article
Females of the obligately parasitic cuckoo ant,Leptothorax kutteri, a workerless inquiline, are among the only adult ants that can successfully invade ant societies and come to be accepted as a nestmate by the existing adult workers. This occurs even though the cuckoo ant is usually severely attacked by theLeptothorax acervorum workers of the colony that she is attempting to enter and parasitize. Through extensive ethogram studies of established parasites and parasitized and free-livingL. acervorum workers and queens, we show that theL. kutteri queen grooms host queens at an exceptionally high frequency. Possibly associated with this behavior, the established parasite is never attacked by theL. acervorum workers or queens she exploits. We show that there is exceptional similarity between the cuticular hydrocarbons and especially the cuticular fatty acids of the parasitic females and her nestmateL. acervorum workers, compared with nonnestmate workers and queens. We suggest that this matching of cuticular compounds may be associated with the grooming of host queens by the parasite. This in turn suggests the possibility that fatty acids have a role in colony-specific nestmate recognition in these and other ants and that grooming may serve for the dissemination of such substances throughout the colony.