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Low intraspecific aggression level in the polydomous and facultative polygynous ant Ectatomma tuberculatum

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Nestmate recognition is a key feature of social insects, as it preserves colony integrity. However, discrimination of non-nestmates and nestmate recognition mechanisms are highly variable according to species and social systems. Here, we investigated the intraspecific level of aggression in the facultative polygynous and polydomous ant, Ectatomma tuberculatum Olivier (Hymenoptera: Formicidae: Ectatomminae), in a population with a strong genetic structure. We found that the intraspecific level of aggression was generally low in this population of E. tuberculatum. However, the level of aggression was significantly correlated with the geographical distance, suggesting that both genetic and environmental cues could be involved in nestmate recognition and discrimination mechanisms. Moreover, polydomy was confirmed by the absence of aggression between workers from nests at a distance of 3 m, while the level of aggression was significantly higher between workers from nests separated by a distance of 10 or 1300 m. Field experiments showed that the low level of aggression between neighbouring colonies was associated with shared foraging areas, which could suggest that familiarization processes may occur in this species. We propose that the particular social organization of this species, with secondary polygyny, polydomy, and budding, may have favoured a high acceptance threshold, because of the low probability of interactions with unrelated conspecifics, the high cost of erroneously rejecting nestmates, and the low cost of accepting non-nestmate workers. The resulting open recognition system can thus allow privileged relationships between neighbouring colonies and promote the ecological dominance of E. tuberculatum in the mosaic of arboreal ants.
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© 2008 The Authors
Entomologia Experimentalis et Applicata
126
: 211–216, 2008
Journal compilation © 2008 The Netherlands Entomological Society
211
DOI: 10.1111/j.1570-7458.2007.00654.x
Blackwell Publishing Ltd
Low intraspecific aggression level in the polydomous
and facultative polygynous ant
Ectatomma tuberculatum
L. Zinck
1
*, R.R. Hora
2†
, N. Châline
1
& P. Jaisson
1
1
Laboratoire d’Ethologie Expérimentale et Comparée (UMR CNRS 7153), Université Paris 13, 99 Avenue J.-B. Clément,
93430 Villetaneuse, France;
2
Laboratório de Mirmecologia, Centro de Pesquisas do Cacau, C.P.7, Itabuna, Bahia, Brazil
Key words
: Hymenoptera, Formicidae, nestmate recognition, discrimination, acceptance threshold,
territoriality, polygyny, polydomy, unicoloniality
Accepted: 8 November 2007
Abstract
Nestmate recognition is a key feature of social insects, as it preserves colony integrity. However,
discrimination of non-nestmates and nestmate recognition mechanisms are highly variable according
to species and social systems. Here, we investigated the intraspecific level of aggression in the
facultative polygynous and polydomous ant,
Ectatomma tuberculatum
Olivier (Hymenoptera:
Formicidae: Ectatomminae), in a population with a strong genetic structure. We found that the
intraspecific level of aggression was generally low in this population of
E. tuberculatum
. However, the
level of aggression was significantly correlated with the geographical distance, suggesting that both
genetic and environmental cues could be involved in nestmate recognition and discrimination
mechanisms. Moreover, polydomy was confirmed by the absence of aggression between workers from
nests at a distance of 3 m, while the level of aggression was significantly higher between workers from
nests separated by a distance of 10 or 1300 m. Field experiments showed that the low level of aggression
between neighbouring colonies was associated with shared foraging areas, which could suggest that
familiarization processes may occur in this species. We propose that the particular social organization
of this species, with secondary polygyny, polydomy, and budding, may have favoured a high acceptance
threshold, because of the low probability of interactions with unrelated conspecifics, the high cost of
erroneously rejecting nestmates, and the low cost of accepting non-nestmate workers. The resulting
open recognition system can thus allow privileged relationships between neighbouring colonies and
promote the ecological dominance of
E. tuberculatum
in the mosaic of arboreal ants.
Introduction
The world-wide ecological success of ants is greatly due to
their social organization (Hölldobler & Wilson, 1990).
Colony members exhibit complementary social behaviours
that result in overall colony development. The colony
integrity depends on privileged relationships between
individuals of the social group and on their ability to
recognize group members (Crozier & Pamilo, 1996).
Recognition is based on colony odour components that are
influenced both by endogenous and exogenous factors
(Vander Meer & Morel, 1998; Lenoir et al., 1999). Indeed,
individuals of the same colony are generally close relatives,
which live in the same nest (i.e., nestmates). The Gestalt
theory postulates that these colony odour components are
exchanged between nestmates through social interactions
in order to constitute a global template used as a reference
to discriminate nestmates from non-nestmates (Crozier &
Dix, 1979; Soroker et al., 1994; Lenoir et al., 2001). This
model thus explains how nestmate recognition can exist in
colonies where individuals have a different genetic origin,
such as in polygynous species (i.e., where colonies contain
several reproducing queens). A more complex situation is
found in polydomous species where colonies are formed of
several physically separated nests and of individuals living
*
Correspondence: Lea Zinck, Laboratoire d’Ethologie Expérimentale
et Comparée (UMR CNRS 7153), Université Paris 13, 99 Avenue J.-B.
Clément, 93430 Villetaneuse, France.
E-mail: lea.zinck@leec.univ-paris13.fr
Present address: Departamento de Biologia Geral, Universidade
Federal de Viçosa, Viçosa 36570-000, Minas Gerais, Brazil.
L. Zinck and R.R. Hora contributed equally to this article.
212
Zinck
et al.
in different environments. However, as polydomy is
associated with continuous worker exchange between
nests, a colony mate recognition can exist between
non-nestmate workers that belong to the same colony
(Stuart & Herbers, 2000).
In this study, we investigated the intraspecific level of
aggression in
Ectatomma tuberculatum
Olivier (Hymenoptera:
Formicidae: Ectatomminae), a neotropical ant with a
complex social organization and genetic structuring.
Ectatomma tuberculatum
is characterized by a facultative
polygyny, as its nests can contain either one or several
queens (Hora et al., 2005b). However, monogyny was
shown to be rare in the population studied. Polygyny
resulted in highly variable relatedness values between
nestmate workers, ranging from r = 0 to r = 0.74 (Zinck
et al., 2007). In contrast, the existence of both polydomy
and budding (i.e., colony foundation by a queen and a
group of workers in the proximity of their natal nest)
allows the maintenance of a strong population genetic
structure, with distant nests being more genetically differ-
entiated than neighbouring ones (Zinck et al., 2007).
Thus, while nestmate recognition based on genetic cues
could lead to important errors of discrimination, an
efficient colony mate recognition could result from a
recognition system based on genetic cues. We thus con-
ducted dyadic aggression tests first to study behavioural
boundaries between colonies and to determine whether
workers discriminate nestmates from non-nestmates, and
colony mates from non-colony mates. Moreover, because
E. tuberculatum
is ecologically dominant in the mosaic of
arboreal ants, with nests that are typically aggregated in
patches (Majer et al., 1994; Medeiros et al., 1995), we
studied patterns of aggression between nests within and
between patches, to investigate the relationships existing
between nests. Second, we investigated foraging behaviour
and levels of aggression in the field to find out the occurrence
of territoriality in
E. tuberculatum
. Indeed, given that nests
in this species are stable structures established at the base
of trees on which workers forage, these trees could be
actively defended against alien conspecifics (Weber, 1946;
Delabie, 1990; Figure 1).
Materials and methods
The study was conducted in cocoa plantations of the
Centro de Pesquisas do Cacau (CEPEC/CEPLAC) in Itabuna,
Bahia (14
°
48
W, 3 9
°
16
S), Brazil.
Ectatomma tuberculatum
workers typically build their nest at the basis of a tree,
along the main root and they construct a visible 10–30-cm
long chimney at the nest entrance using organic materials
(Delabie, 1990; Figure 1), which allows clear nest
identification. Because of the occurrence of polydomy in
this species (Hora et al., 2005b; Zinck et al., 2007), several
of these nests can form a single colony. We will thus use the
term ‘nest’ to refer to the physical aspect (Figure 1) whereas
the term ‘colony’ will be use to refer specifically to the
functional feature, which can be composed of either one or
several physical nests.
Dyadic aggression tests of 5 min were performed
directly after collection, using 2.5 cm diameter Petri
dishes. To analyze the effect of nest distance on intraspecific
aggression, we performed tests between pairs of workers
originating from nests separated by a distance of either 0
(control), 3, 10, or 1300 m, and 17 km. The tests were
repeated 10 times for each distance with different pairs of
nests and again 10 times for each pair of nests with new
workers (n = 500) to control for internest and inter-
individual variation, respectively. Following standard
protocols (Holway et al., 1998; Suarez et al., 1999; Giraud
et al., 2002; Tsutsui et al., 2003), we scored the highest level
of aggression for each test: 0, ignorance (physical antennal
contact without aggression); 1, opening mandibles
(opening mandibles without biting); 2, biting (biting a leg
or the head of a worker), and 3, stinging (one worker bites
and stings the other). As our data are not independent
Figure 1 Ectatomma tuberculatum nest structure (from Delabie,
1990 with the authorization of the author).
Low aggression level in
Ectatomma tuberculatum
213
replicates, we performed a hierarchical analysis of variance
(ANOVA) with repeats of workers from the same nest
nested in the different pairs of nests to compare the mean
level of aggression obtained for each distance (i.e., 0, 3, 10,
and 1300 m, and 17 km) using Statistica 6.1 (StatSoft Inc.,
Tulsa, OK, USA). Non-parametric permutation tests, with
repeats of workers from the same nest blocked, were used
to make two-by-two comparisons (Good, 2000), and a
sequential Bonferroni correction (Holm, 1979) was applied
to the StatXact-3 (Cytel Software Corporation, Cambridge,
MA, USA) obtained P-value. Pearson’s correlation coefficient
was calculated between the mean score of aggression found
for each pair of nests and the geographical distance between
nests and tested for no association using StatXact-3.
To investigate non-nestmate workers’ interactions in the
field, we studied foraging behaviour to determine if each
nest had its own territory or if neighbouring nests shared
a common foraging area. We studied nine groups of nests,
each one consisting of six neighbouring nests (n = 54).
The nests within a group were separated by 3– 6 m. For
each group of nests, foragers found on a given tree were all
marked with the same enamel paint colour and a different
colour was used for each tree. A total of 3405 foragers were
marked, with an average of 63.9 (± 43.9) workers per nest.
On the following 2 days (2.5 h/day), two observers checked
the six trees of the group being studied, and recaptured all
the marked foragers found. Foragers with a different
colour than expected (i.e., coming from neighbouring
trees) were not released, in order to prevent counting the
same ant exchange twice. This procedure permitted to spot
the workers foraging on a tree distinct from their nest tree,
either when they were marked or when they were recaptured.
The degree of overlap between the foraging domains of
neighbouring nests was estimated by the ratio of the
number of workers from other trees upon the total
number of marked workers recaptured per tree, for each
day. The mean ratio gave us an estimation of the average
percentage of worker exchanges per day.
Results
The intraspecific level of aggression was found to be
generally low in
E. tuberculatum
. Stinging was only
recorded between workers coming from nests at 17 km
distance, but even over this distance, the mean level of
aggression was low as a score of 1, only corresponds to a
worker opening its mandibles (averaged median = 1.05,
range: 0.3–1.4; Figure 2). However, the level of aggression
was significantly correlated with the geographical distance
[Pearson’s correlation test: Rp = 0.573, 95% confidence
interval (CI): 0.353–0.792, and P<0.0001] and significant
differences in the level of aggression were found depending
on the geographical distance between nests (ANOVA:
F = 2.88, d.f. = 45, and P<0.0001; Figure 2). The level of
aggression was not significantly different between workers
from nests at a distance of 3 m and between nestmates,
while it was significantly higher between workers from nests
at 10 m distance than between nestmates (Permutation
tests: n = 100, P = 0.1455 and P = 0.0001, respectively)
(Figure 2). However, the level of aggression between nests
at a distance of 3 and 10 m did not differ significantly after
a sequential Bonferroni correction (Holm, 1979), which
lowered the significance level of
α
= 0.05 to
α
i = 0.0167
for this pairwise comparison (Permutation tests: n = 100,
P = 0.0257, not significant after sequential Bonferroni
adjustment) (Figure 2).
Foragers with a different colour, coming from one to
several neighbouring nests, were found on trees of eight
groups out of nine. Over the 54 trees and the 3405 marked
foragers, 119 workers were recorded foraging on neighbouring
trees out of a total of 1558 marked workers recaptured. The
maximum distance at which we found a worker was 14 m
from its nest of origin. On average, over all groups, 7.09%
(±7.74) of the marked workers foraged on trees where
other nests were established each day.
Discussion
Overall, the intraspecific aggression level between
E. tuberculatum
workers was low. However, significant
Figure 2 Results of dyadic aggression tests (n = 500). Ten
repetitions with different workers from the same nest were used
to calculate the mean level of aggression between pairs of nests
and the median was calculated for each distance using 10 different
pairs of nests. Squares indicate the median values, box ends
represent the 25 and the 75th percentiles, error bars the 10 and
90th percentiles, and circle and star indicate atypical and extreme
values, respectively. Different letters correspond to significant
permutation tests with sequential Bonferroni correction.
214
Zinck
et al.
differences in the level of aggression between workers
suggest that recognition and discrimination abilities exist
in
E. tuberculatum
. Previous results of aggression tests
performed between
E. tuberculatum
workers coming from
Brazilian vs. Mexican populations also revealed the ability
of this ant to discriminate (Fénéron et al., 1999), but nestmate
recognition was not investigated within each of these
populations. Our results revealed that the level of aggression
in
E. tuberculatum
was correlated with the geographical
distance between nests, suggesting that both genetic and
environmental cues might be used for this discrimination.
Indeed, this population of
E. tuberculatum
has been shown
to be strongly genetically structured with a significant
isolation by distance, that is, with distant nests being more
genetically differentiated than neighbouring ones (Zinck
et al., 2007). Moreover, genetic and/or environmental cues
are known to play a role in nestmate recognition in other
polygynous ant species (e.g.,
Formica polyctena
: Beye et al.,
1997;
Formica pratensis
: Beye et al., 1998; Pirk et al., 2001;
Leptothorax longispinosis
: Stuart & Herbers, 2000).
The level of aggression between workers from nests at a
distance of 3 m was not significantly higher than the level
of aggression found between nestmate workers (i.e., 0 m;
Figure 2). This, therefore, confirms the existence of
polydomy in
E. tuberculatum
(Zinck et al., 2007). Moreover,
our results showed that the level of aggression between
nests that did not belong to the same polydomous colony,
at either 10 or even 1300 m distance, remained surprisingly
low. This low aggression between workers from different
colonies can hardly be explained by environmental
similarity due to nearby homogenized habitats, or by
genetic similarity that results from budding (i.e., colony
foundation by a queen and a group of workers in the
proximity of their natal nest). Indeed, such explanations
could not reasonably explain the low level of aggression
found between workers from nests of different patches of
habitat (i.e., at a distance of 1300 m), which are known to
be genetically differentiated (Zinck et al., 2007). As learning
and familiarization are known to be involved in nestmate
recognition (Jaisson, 1991; Crozier & Pamilo, 1996), such
processes could explain the low level of aggression found
between workers from nests separated by 10 m. Indeed,
our field experiment on
E. tuberculatum
territoriality
showed that foragers from different nests (and probably
different colonies) shared the same foraging area, and
repeated interactions between foragers of neighbouring
colonies have already been shown to lead to low levels of
aggression due to habituation (Langen et al., 2000). However,
our results do not prove that familiarization actually
occurs in
E. tuberculatum,
and habituation still may not
explain the absence of aggression between unfamiliar
workers coming from nests at a distance of 1300 m.
Our results thus suggest that the low level of aggression
in
E. tuberculatum
may be due to low discrimination that
could result from a high acceptance threshold (Reeve,
1989). We propose that this low discrimination in
E. tuberculatum
could have been favoured by the secondary
polygyny, polydomy, and the colony reproduction by
budding that characterize this species. Indeed, secondary
polygyny is associated with a high variability in nestmate
relatedness and queen number per nest in
E. tuberculatum
(Zinck et al., 2007), which makes the use of genetic cues to
discriminate nestmates from non-nestmates unreliable.
Similarly,
E. tuberculatum
workers cannot rely on environ-
mental cues for this discrimination because of polydomy.
Thus, neither genetic nor environmental components
alone allow a reliable and accurate discrimination between
colony mates and non-colony mates in this species. In
contrast, colony reproduction by budding gives rise to
genetic viscosity and to a high relatedness between nei ghbou r-
ing nests, which could have favoured the evolution of high
acceptance thresholds. Genetic viscosity indeed decreases
the costs associated with non-nestmate acceptance, as
non-nestmates that can interact are likely to be related.
Moreover, the absence of aggression between neigh-
bouring colonies could result in a better colony growth, as
non-aggressive interactions between colonies have been
shown to result in a higher foraging activity and a lower
mortality compared to aggressive pairs of colonies in the
Argentine ant
Linepithema humile
(Holway et al., 1998).
Similar benefits at the colony level, resulting in increased
colony growth, can also explain the lack of territoriality
that we observed in
E. tuberculatum
. The low level of
aggression between neighbouring colonies and the
absence of territoriality in
E. tuberculatum
could thus
actually contribute to the ecological dominance of the
species in the mosaic of arboreal ants (Majer et al., 1994).
Interspecific competition is indeed known to be particularly
strong in these habitats (Majer, 1972; Leston, 1973; Majer,
1976). Reduced levels of aggression might have therefore
been favoured in
E. tuberculatum
by the low probability
of interactions with unrelated conspecifics, the high cost
of erroneously rejecting nestmates, and the low cost of
accepting non-nestmate workers (Reeve, 1989). Inter-
estingly, the same hypothesis was proposed to explain the
low levels of aggression found in the unicolonial ant
Formica paralugubris
(Chapuisat et al., 2005). Indeed, low
aggression levels generally characterize unicolonial ants,
which form supercolonies with no behavioural boundaries
between colonies (Hölldobler & Wilson, 1990). However,
most of these species are invasive and their absence of
intraspecific aggression and territoriality is usually
attributed to a loss of genetic diversity during introduction
(e.g., Suarez et al., 1999; Tsutsui et al., 2003). In
Low aggression level in
Ectatomma tuberculatum
215
E. tuberculatum
, the occurrence of polygyny, polydomy,
and budding can explain the evolution of low intraspecific
aggression level between non-nestmates as well as the
absence of territoriality. Although these features are used
to define unicolonial species (Hölldobler & Wilson, 1990),
E. tuberculatum
cannot actually be considered as unicolonial,
because its colonies are kin-structured, due to a limited
number of queens per nest (Zinck et al., 2007). Thus, even
if low intraspecific aggression in
E. tuberculatum
allows the
existence of privileged relationships between workers from
neighbouring colonies, as revealed by our territoriality
experiment, it is not linked to unicoloniality.
In conclusion, our results show that intraspecific aggres-
sion is low in
E. tuberculatum
and that this species is not
territorial. The particular breeding system and life-history
traits of
E. tuberculatum
(i.e., secondary polygyny, polydomy,
and budding) may have favoured the existence of high
acceptance thresholds that results in such an open recogni tion
system. We propose that the ecological dominance of
E. tuberculatum
in the mosaic of arboreal ants partly stems
from this open recognition system even if it may also
favour the emergence of intraspecific social parasitism.
Cheater strategies could indeed more easily emerge in such
species, in which workers are not aggressive towards alien
conspecifics. Social parasitism seems to be likely in
Ectatomma
species, as the behaviour of cleptobiosis, that
is, the robbing of food from another nest, was already
shown to exist in
Ectatomma ruidum
(Perfecto & Vandermeer,
1993; Breed et al., 1999), and parasitic queens have been
found in Mexican populations of
E. tuberculatum
(Hora
et al., 2005a). However, the benefits associated with the
occurrence of an open recognition system may outweigh
the costs and possible risks associated with it.
Acknowledgements
We thank D. Denis for his advice on statistical analysis;
C. Doums for comments on an earlier version; J.H.C.
Delabie for providing the illustration; the CEPLAC staff for
their support of the field work; and two anonymous
referees for their helpful comments on the manuscript.
This study was supported by the Université Paris 13 inter-
national office. R.R. Hora received financial support from
CNPq, Brazil (3098552003-9). This research was permitted
by the Brazilian Minister of Science and Technology
(licence no. 0107/2004).
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. Behavioral
Ecology 18: 701–708.
... Esta distribuição em manchas, combinada com a ausência de rainhas em muitas colônias amostradas, dão indícios à polidomia (formação de ninhos múltiplos espacialmente isolados que podem trocar operárias e a prole) (DEBOUT et al., 2007). A polidomia é sugerida em outras espécies como E. brunneum (LAPOLA et al., 2003;ANTONIALLI-JUNIOR, 2006), e E. opaciventre (TOFOLO et al., 2014), mesmo que a presença da rainha em menos de 20% dos ninhos coletados tenha sido resultado de uma escavação incompleta devido a estrutura do solo que não permitiu que as câmaras mais profundas fossem encontradas em ambas as espécies, mas comprovada apenas em E. tuberculatum (ZINCK et al., 2007(ZINCK et al., , 2008. Detalharemos mais precisamente a dispersão de E. tuberculatum e E. ruidum em sua área de distribuição abaixo. ...
... Por outro lado, a ausência de endogamia em E. tuberculatum sugere que a dispersão de machos não é tão restrita quanto a dispersão de fêmeas. Além disso, os registros genéticos e resultados de experimentos comportamentais em campo (ZINCK et al., 2008) tendem a confirmar a polidomia nesta espécie, algo sugerido anteriormente por diferentes autores (GARCÍA-PÉREZ et al., 1991;HORA et al., 2005a) e ninhos que possam permanecer interligados após fissão, por meio do intercâmbio de operárias como em outras espécies (CHAPUISAT et al., 1997;PEDERSEN;BOOMS-MA, 1999). Em conclusão, para as espécies brasileiras, a combinação de diferentes características biológicas como a poliginia secundária, a reprodução por fissão e polidomia contribui para a manutenção de sua dominância ecológica no mosaico de formigas arbóreas. ...
... Like other social insects, Ants show a high degree of cooperation among the individuals that interact in the colony (Zinck et al., 2008). For instance, workers play an active role in nest construction, colony protection against predators, foraging, and brood care (Ratnieks et al., 2006). ...
Article
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The aim of the present paper is to study magnetosensibility and to seek for magnetic nanoparticles in ants. The social insects, by living in colonies, developed very efficient methods of nestmate recognition, being less tolerant towards individuals from other colonies. Therefore, any kind of strange behavior between nestmates and/or conspecifics, besides those present in their own behavioral repertoire, is not expected. The behavior study in the present paper analyze whether changes in the intensity of applied magnetic fields on Ectatomma brunneun (Smith) ants can cause changes in the normal pattern of interaction between conspecifics. A pair of coils generating a magnetic field was used to change the whole local geomagnetic field. Magnetometry studies were done on abdomens and head + antennae using a SQUID magnetometer. The results show that changes in the geomagnetic field affect the usual pattern of interactions between workers from different colonies. The magnetometry results show that abdomens present superparamagnetic nanoparticles and heads present magnetic single domain nanoparticles. Behavior experiments show for the first time that Ectatomma brunneun ants are magnetosensible. The change in nestmate recognition of Ectatomma ants observed while a magnetic field is applied can be associated to some kind of disturbance in a magnetosensor presented in the body based on magnetic nanoparticles.
... In the specific case of polydomous ant colonies, which consist of multiple socially connected but spatially separated nests (see Helanterä et al. 2009;Markó et al. 2012;Robinson 2014), one would expect a small increase in the level of aggression with an increase in the distance between the nests, with aggression peaking eventually among individuals from distant nests (Zinck et al. 2008). In polydomous systems there is a frequent exchange of individuals and information among neighboring nests, and food source sharing is common (e.g. ...
Article
Intra‐ and interspecific aggression is quite common in ants, from occasional conflicts to large‐scale territorial disputes. The “nasty neighbor” phenomenon describes the differential aggressive treatment of neighbors versus foreign intruders. Due to the fact that workers of a given colony meet rival neighbors more often at food resources, they treat them as threats to their colony. The reverse can also happen: the “dear enemy” effect arises when an already known rival is treated less aggressively due to accommodation, than an unknown distant one. In the current study, we analyzed the effect of distance on the aggressiveness of Liometopum microcephalum, a territorial arboricolous ant, towards non‐nestmates in two large populations. Our results show that aggression did not increase with distance, but it was higher among neighbors than among workers coming from distant nests. The results of the study are consistent with the nasty neighbor scenario, and do not support the hypothesis that the studied populations would be polydomous systems of interconnected nests.
... Our supercolonial site may indeed consist of multiple supercolonies instead of one, but the lack of clear patterns and the overall low levels of aggression revealed in our study ( Figure 5) lend little support to the existence of clear and persistent borders at our study site. Finally, aggression has been shown to increase with internest distance also in monodomous species (Beye, Neumann, Chapuisat, Pamilo, & Moritz, 1998) and among distinct colonies or sites Pirk, Neumann, Moritz, & Pamilo, 2001;Rosengren, Cherix, & Pamilo, 1986;Zinck, Hora, Châline, & Jaisson, 2008), making these kinds of behavioral patterns hard to interpret. ...
Thesis
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http://urn.fi/URN:ISBN:978-951-51-5973-1 There are intricate links between the evolution of sociality and the spatial population structures created by dispersal. In ants, the evolution of the most complex societies, supercolonies, is strongly connected to limited dispersal. The supercolonies consist of hundreds of interconnected nests where thousands of queens and their workers cooperate over large areas. Supercolonies arise from simpler family units when large proportions of daughter queens are philopatric and stay in their natal colony as additional reproducing queens instead of dispersing by wing. This allows the colonies to grow quickly and colonize large areas, but also increases social conflicts due to very low local relatedness in these societies. In this thesis I inspect the evolution and maintenance of ant supercolonies, by focusing on dispersal traits and the consequences of dispersal in socially polymorphic Formica ants. Formica have both simple family-based monodomous colonies and complex supercolonies, and some species have also intraspecific variation. To lay a sound theoretical background for my work, I began by synthesizing current knowledge of dispersal evolution in ants. In my literature review I showed how eco-evolutionary feedbacks link the evolution of ant dispersal strategies and social organization, and pinpointed the most relevant future research directions. Next, to be able to inspect some of the hypotheses formulated in the review, I clarified the species identification of one of my intended study species, Formica fennica with molecular methods, and concluded that the populations I studied should be treated as conspecific to Formica exsecta. I analyzed the individual dispersal traits of six socially variable species of Formica ants to assess whether dispersal ability varies between monodomous and supercolonial societies in accordance to the observed behavioral difference. According to my results the dispersal behavior of these species is likely not restricted by their morphology or resources the individuals get from their natal colonies. The traits of all species and both sexes indicate good flight ability, with overall male bias and large variation both among and within species. The increased philopatry in supercolonial species and populations is more a behavior change: the queens are philopatric even though the society provides them resources for dispersal. However, I observed a small decrease of male flight muscle ratio in supercolonial species, which indicates strong coevolution of the sexes. In order to better understand the outcomes of limited dispersal in supercolonial Formica, I analyzed the behavioral and genetic structure of a dense supercolonial population of Formica pressilabris. The population is genetically viscous at a small spatial scale, but still not genetically structured by location on a larger spatial scale. This indicates that although dispersal is limited within the population, a large enough proportion of individuals do disperse to keep the local populations connected. Interestingly, when analyzing worker behavior among the polydomous nests, the observed aggression pattern indicates that they are not a single cooperative unit – but also not clearly separate colonies. The sensitive behavioral assay developed for this study shows that workers allow a proportion of individuals from outside nests to enter their own nest material, but are slightly more aggressive towards individuals from further away. This indicates the population is only partially cooperative over the whole nest aggregation, and shows that the inner structures of supercolonies should be analyzed in more detail. This thesis sheds light on ants’ dispersal ability and behavior, and demonstrates the crucial role of dispersal in the evolution of their different social structures. My results also raise new questions about possible conflicts over dispersal in ant societies.
... Our supercolonial site may indeed consist of multiple supercolonies instead of one, but the lack of clear patterns and the overall low levels of aggression revealed in our study ( Figure 5) lend little support to the existence of clear and persistent borders at our study site. Finally, aggression has been shown to increase with internest distance also in monodomous species (Beye, Neumann, Chapuisat, Pamilo, & Moritz, 1998) and among distinct colonies or sites (Holzer et al., 2006;Pirk, Neumann, Moritz, & Pamilo, 2001;Rosengren, Cherix, & Pamilo, 1986;Zinck, Hora, Châline, & Jaisson, 2008), making these kinds of behavioral patterns hard to interpret. ...
Article
Full-text available
Understanding how social groups function requires studies on how individuals move across the landscape and interact with each other. Ant supercolonies are extreme cooperative units that may consist of thousands of interconnected nests, and their individuals cooperate over large spatial scales. However, the inner structure of suggested supercolonial (or unicolonial) societies has rarely been extensively studied using both genetic and behavioral analyses. We describe a dense supercolony‐like aggregation of more than 1,300 nests of the ant Formica (Coptoformica) pressilabris. We performed aggression assays and found that, while aggression levels were generally low, there was some aggression within the assumed supercolony. The occurrence of aggression increased with distance from the focal nest, in accordance with the genetically viscous population structure we observe by using 10 DNA microsatellite markers. However, the aggressive interactions do not follow any clear pattern that would allow specifying colony borders within the area. The genetic data indicate limited gene flow within and away from the supercolony. Our results show that a Formica supercolony is not necessarily a single unit but can be a more fluid mosaic of aggressive and amicable interactions instead, highlighting the need to study internest interactions in detail when describing supercolonies. We study behavior and genetic structure in a dense supercolony‐like aggregation of more than 1,300 ant nests. Aggression bioassays reveal some aggression within the assumed supercolony, but there are no clear colony borders. The occurrence of aggression increases with distance from the focal nest, in accordance with the genetically viscous population structure we observe by using 10 microsatellite markers.
... The behaviors elicited by contact with the chemical profiles of colony-mate or foreign workers functionally determine colony boundaries [23,24]. The intraspecific aggressive behaviors triggered by contact with foreign workers vary considerably among ant species [25][26][27][28] and interaction context [29][30][31]. In the case of N. fulva, in North America intraspecific aggression in a neutral arena context has been noted to be absent both within [32] and between [15] local populations. ...
Article
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How workers within an ant colony perceive and enforce colony boundaries is a defining biological feature of an ant species. Ants fall along a spectrum of social organizations ranging from single-queen, single nest societies to species with multi-queen societies in which workers exhibit colony-specific, altruistic behaviors towards non-nestmate workers from distant locations. Defining where an ant species falls along this spectrum is critical for understanding its basic ecology. Herein we quantify queen numbers, describe intraspecific aggression, and characterize the distribution of colony sizes for tawny crazy ant (Nylanderia fulva) populations in native range areas in South America as well as in their introduced range in the Southeastern United States. In both ranges, multi-queen nests are common. In the introduced range, aggressive behaviors are absent at all spatial scales tested, indicating that within the population in the Southeastern United States N. fulva is unicolonial. However, this contrasts strongly with intraspecific aggression in its South American native range. In the native range, intraspecific aggression between ants from different nests is common and ritualized. Aggression is typically one-sided and follows a stereotyped sequence of escalating behaviors that stops before actual fighting occurs. Spatial patterns of non-aggressive nest aggregation and the transitivity of non-aggressive interactions demonstrate that results of neutral arena assays usefully delineate colony boundaries. In the native range, both the spatial extent of colonies and the average number of queens encountered per nest differ between sites. This intercontinental comparison presents the first description of intraspecific aggressive behavior for this invasive ant and characterizes the variation in colony organization in the native-range, a pre-requisite to a full understanding of the origins of unicoloniality in its introduced range.
... Although each colony had its own chemical signature as suggested by studies on CHCs in other ant species, such as A. senilis (Lenoir et al., 2001) and Ectatomma vizottoi Almeida (Formicidae: Ectatomminae) (Antonialli-Junior et al., 2007), there is greater similarity between profiles of colonies nested in nearby sites. One possible explanation is the higher level of kinship between these colonies due to a restricted dispersal strategy and/or by the phenomenon of colony fission already documented for E. tuberculatum Olivier (Formicidae: Ectatomminae) (Zinck et al., 2008). On the other hand, it is well known that CHCs composition is determined by two main components: genetic and environmental (Sorvari et al., 2008), thus this similarity in CHCs profile, as well as the low level of aggression, might be partially explained by environmental similarity, especially microhabitats shared by neighboring colonies. ...
Article
Full-text available
The integrity of ant colonies depends exclusively on social relatonships between their individuals, especially the ability of communicaton between group members, which is mainly mediated through chemical signals. Another important feature of ant behavior is territory defense, since they need to gather large amounts of food to feed their larvae, males and breeding females. Thereby, ants might display behavioral strategies to defend their territories from intruders. Here we investgated whether Ectatomma brunneum displays the Dear Enemy Phenomenon, what is the relatonship between Cutcular Hydrocarbon compositon and levels of aggression during their intraspecifc interactons and which compounds and/or classes of compounds might be the most important to modulate the level of aggression. To test our hypothesis, we evaluated the levels of aggression through behavioral observatons during interactons between 23 pairs of colonies nested in two distnct sites at varied distances. Then, we analyzed the cutcular chemical profle of the individuals involved in the interactons, and compared these results with the levels of aggression displayed between colonies tested. The results allow us to confrm our hypothesis that the DEP occurs in E. brunneum. The higher tolerance between closer colonies can be explained due to their kinship level in additon to sharing the same microhabitats. The results also showed there are signifcant differences in CHCs profles, especially between colonies nested at relatvely greater distances, and it is likely that differences in content of some branched alkanes are the most important to establish these differences and, therefore, the levels of aggression during the interactons
... Hierarchical models that match the nested structure of the data (Gelman & Hill, 2007;Zuur et al., 2009) are well suited for this kind of analysis and are becoming more common in studies on social insect aggression (e.g. Zinck et al., 2008;Gill et al., 2012;Yagound et al., 2017). We used Bayesian hierarchical models (Gelman & Hill, 2007), estimating random effects at the level of the nest and the assay to account for colony-level variation in aggression and overdispersion in counts of fighting ants. ...
Article
1. Patterns of aggression between ants from different nests influence colony and population structure. Several species of invasive ants lack colony boundaries over large expanses, forming ‘supercolonies’ with many nests among which workers can move without encountering aggression. 2. Bioassays of aggression were used to determine the colony structure of the invasive ant Myrmica rubra (L.) at eight sites in Massachusetts, the state where the species was first discovered in North America. To improve the ability to distinguish systematic patterns from background variability in aggressiveness, a repeated‐measures design was used and replicate assays for each pair of nests were conducted. 3. Aggressive responses showed that populations at all sites consisted of multiple distinct colonies. Patterns of aggression were repeatable and transitive, with few exceptions. Colonies were identified as clusters of nests whose workers showed little to no aggression towards one another but were aggressive towards conspecifics from more distant nests. 4. The degree of aggression varied considerably among different colony pairs but did not depend in any consistent way on the distance of separation or on whether colonies were neighbours. 5. Territories of neighbouring colonies abutted, indicating that they were restricted by intraspecific competition. Mapped territories ranged in size from 0.03 to 1.2 ha, but colonies at the study sites have not undergone the enormous expansions seen in introduced populations of some other species of invasive ants, and neighbouring colonies compete locally.
... Because colonies vary in aggressiveness, replicates using the same colony are likely to have correlated outcomes and failing to take this into account during the analysis can result in pseudoreplication. Hierarchical models that match the nested structure of the data ) are well suited for this kind of analysis but are not often used in studies on social insect behavior (but see Zinck et al. 2008, Gill et al. 2012. We used Bayesian hierarchical models, estimating random effects at the level of the nest and the assay to account for variation in aggression and overdispersion in counts of fighting ants (Gelman and Hill 2007). ...
Article
The Eurasian ant Myrmica rubra L. was first discovered in North America in the early 1900s in Boston and Woods Hole, Massachusetts, and is now established across large parts of the northern United States and Canada. Its aggressive behavior, painful sting and high local population densities make it a potentially serious pest to local residents and a threat to biodiversity. I studied the distribution, habitat affinities, and population structure of this species across southern New England. A systematic search showed that M. rubra is widespread in the Greater Boston area and the Berkshires range, with smaller populations elsewhere in Massachusetts and Rhode Island. The ant was not detected in Connecticut or across large expanses of central Massachusetts and northern Rhode Island, despite the presence of suitable habitat. This distribution suggests a combination of long-distance dispersal mediated by humans coupled with slow local spread. Analysis of mitochondrial DNA revealed multiple haplotypes that are shared with populations in central Europe. Invasive species distribution modeling is complicated by the fact that many introduced species are not yet in equilibrium with their environment. To address this challenge, a Bayesian hierarchical approach was employed that combines two components: a spatial model, allowing estimation of the geographic extent of the invasion, and a habitat suitability model, quantifying the association between several environmental predictors and the presence of the ant. The spatial component describes uncertainty in where the ant has arrived and can account for spatial dependence in outcomes at nearby locations. This approach discounts the contribution of sites where the species has not arrived to estimation of the habitat suitability model. M. rubra was more likely to be found at sites with high amounts of wetland, water, and developed habitat within 300 m, at sites with wetland plants and stands of the invasive Fallopia japonica Houtt (= Reynoutria japonica Houtt or Polygonum cusidatum; Japanese knotweed), and at sites with low maximum temperatures in the hottest month of the year. The ant was most prevalent in marshes, wet meadows, and wet forests and was rarely found in drier forests or in open areas. These results suggest that, within southern New England, M. rubra is limited to places where the soil does not dry out during the summer. Its restriction to these habitats may have contributed to its slow dispersal during the last 115 years. Several widespread and damaging species of invasive ants have populations that lack colony boundaries, or that are characterized by large supercolonies with many nests and queens, such as Linepithma humile (Argentine ant), Wasmania auropunctata (little fire ant) and Anoplepis gracilipes (yellow crazy ant; Holway et al. 2002, Lach and Hooper-Bui 2010). Bioassays of aggression were used to determine colony and population structure of M. rubra at eight sites spanning two major invasions in Massachusetts. Populations at all sites consisted of multiple colonies that were mutually aggressive. The largest colonies can be considered supercolonies, expandable networks of nests distributed across more than a hectare. Hierarchical models, accounting for variation in aggressiveness among colonies and variation in outcomes across replicate assays, were used to analyze patterns of aggression. There was no evidence that aggressive responses depended on distance of separation between colonies or whether colonies were neighbors. Supercolonies were constrained by intraspecific competition and habitat variation and did not achieve the vast sizes seen in introduced populations of some other invasive ants.
Article
Emphasises the behavioural mechanisms which form the obligatory links between kinship and altruistic acts. In examining interspecific associations in ants and social wasps, the author discusses the recognition of phylogenetically distant cues, and describes experimental work which has led to a model for the understanding of the mechanisms and cues involved in nestmate recognition. A table summarises species for which nestmate recognition has been demonstrated. Polistes (wasps) and Camponotus (ants) are used as detailed examples. -P.J.Jarvis
Article
Despite the innumerable ecological problems and large economic costs associated with biological invasions, the proximate causes of invasion success are often poorly understood. Here, evidence is provided that reduced intraspecific aggression and the concomitant abandonment of territorial behavior unique to introduced populations of the Argentine ant contribute to the elevated population densities directly responsible for its widespread success as an invader. In the laboratory, nonaggressive pairs of colonies experienced lower mortality and greater foraging activity relative to aggressive pairs. These differences translated into higher rates of resource retrieval, greater brood production, and larger worker populations.
Article
In unicolonial populations of ants, individuals can mix freely within large networks of nests that contain many queens. It has been proposed that the absence of aggression in unicolonial populations stems from a loss of nest mate recognition, but few studies have tested this hypothesis. We investigated patterns of aggression and nest mate recognition in the unicolonial wood ant, Formica paralugubris. Little aggression occurred, even between workers from nests separated by up to 5 km. However, when aggression took place, it was directed toward non–nest mates rather than nest mates. Trophallaxis (exchange of liquid food) occurred very frequently, and surprisingly, workers performed significantly more trophallaxis with non–nest mates than with nest mates (bias 2.4:1). Hence, workers are able to discriminate nest mates from non–nest mates. Higher rates of trophallaxis between non–nest mates may serve to homogenize the colony odor or may be an appeasement mechanism. Trophallaxis rate and aggression level were not correlated with geographical distance and did not differ within and between two populations separated by several kilometers. Hence, these populations do not represent differentiated supercolonies with clear-cut behavioral boundaries. Overall, the data demonstrate that unicoloniality can evolve despite well-developed nest mate recognition. Reduced levels of aggression might have been favored by the low rate of interactions with foreign workers, high cost of erroneously rejecting nest mates, and low cost of accepting foreign workers. Key words: aggression, discrimination, kin recognition, unicoloniality. [Behav Ecol]
Article
The ability to recognize kin is widespread, and especially important in highly social organisms. We studied kin recognition by assessing patterns of aggression within and between nests of the ant Leptothorax longispinosus. Colonies of this species can be fractionated into subunits, a condition called polydomy. The problem of recognizing relatives is therefore more complex when those relatives can live in two or more different places. We hypothesized that spatial subdivision may have resulted in a stronger genetic component to kin recognition than in cases where colonies live in a single location. To test our hypothesis we assessed recognition capabilities for two populations of this ant that differ in the complexity of their colonies. In a New York, USA, population, polydomy is very common, and colonies also can have multiple queens. By contrast, a population in West Virginia, USA, has colonies that typically are monogynous and rarely are polydomous. We conducted introductions of ants between different nests collected in the same neighborhood, with self-introductions and alien introductions as controls. Nests from the two populations showed corresponding differences in their aggression towards intruders. For New York nests, the extent of genetic similarity was the single best predictor of aggression, whereas for West Virginia nests aggression was jointly influenced by genetic similarity and spatial distance. In both populations, we found nest pairs for which aggression was nonreciprocal; these probably reflect recognition errors by one of the nests. After the ants were maintained in the laboratory for 3 months, their aggression scores rose and fewer recognition errors were made. Thus nest-mate and colony-mate recognition in this species are mediated primarily by endogenous cues (genetic similarity); the importance of exogenous cues for nest mate recognition depends on the population's social system.