Personality of ant colonies (Hymenoptera: Formicidae) - underlying mechanisms and ecological consequences - Biotaxa
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Myrmecological News
ISSN 1997-3500
myrmecologicalnews.org
Myrmecol. News 31: 47-59 doi: 10.25849/myrmecol.news_031:047 27 January 2021
Review Article
Personality of ant colonies (Hymenoptera: Formicidae) – underlying mechanisms
and ecological consequences
Eva Horna-Lowell*, Kevin M. Neumann*, Sean O’Fallon*, Ana Rubio* & Noa Pinter-Wollman
Abstract
Consistent differences in behavior among individual animals, also known as animal personalities, are ubiquitous. In social
insects, there is more than one biological scale at which individuals differ from one another in behavior: workers and
colonies. In most ants, natural selection acts at the level of the colony, therefore differences in collective behavior among
colonies can have important ecological and evolutionary consequences. Here, we review the recent literature on consistent
individual differences among ant colonies in their collective behavior, that is, colony personality. We discuss the causes
and consequences of colony personalities and highlight unanswered questions that can be examined uniquely by studying
ants. We argue that ants are a distinctive study system for examining the links between the mechanisms that underlie
the emergence of personality and the ecological consequences of personalities because of their ability to shape their local
environment, that is, their nest. We end with an example of how the study of colony personality might be applied to identify
solutions for challenges in conservation biology. Overall, the study of ant colony personality opens up new opportunities
for examining the evolutionary history of animal personalities and the feedback between the underlying mechanisms and
ecological consequences of animal personalities.
Key words: Collective behavior, personality, behavioral syndromes, temperament, interactions, review.
Received 24 May 2020; revision received 17 November 2020; accepted 10 December 2020
Subject Editor: Heikki Helanterä
Eva Horna-Lowell, Sean O’Fallon, Ana Rubio & Noa Pinter-Wollman (contact author), Department of Ecology
and Evolutionary Biology, University of California Los Angeles, 621 Charles E. Young Drive South, Los Angeles,
CA 90095, USA. E-mail: nmpinter@ucla.edu
Kevin M. Neumann, Department of Ecology and Evolutionary Biology, University of California Los Angeles,
621 Charles E. Young Drive South, Los Angeles, CA 90095, USA; Program in Ecology, Evolution, and Conservation
Biology, University of Illinois at Urbana-Champaign, 505 South Goodwin Ave., 320 Morrill Hall, Urbana, IL 61801,
USA.
*These authors contributed equally to this work; ordered alphabetically.
Introduction
The study of animal personalities has become a major as collectives, can also differ in their behavior. Here, we
tenet in the field of behavioral ecology over the past two use the term ‘colony personality’ to refer to the consistent
decades. Consistent differences in behavior among individ- collective behaviors of colonies over time and / or across
uals have been referred to as behavioral types, behavioral ecological situations. This use expands the definition of
syndromes, personalities, and temperaments (Sih & al. Sih & al. (2004b) for unitary beings to superorganisms
2004a, b, Réale & al. 2007). Here, we refer to person- (Hölldobler & Wilson 2009) that work collectively
ality as differences in behavior between individuals that towards shared goals. We use the term ‘collective behav-
are consistent over time and / or across situations. These ior’ when we refer to a collective action of a social insect
consistent differences may emerge from different physi- colony that is not necessarily consistent over time and /
ologies and developmental environments and may lead to or situations. Colony personalities can emerge from in-
differences in survival and reproduction. teractions among group members, ontogenetic processes,
In social animals, individual differences in behav- ecological conditions, and other processes (Pinter-
ior can occur at multiple biological scales. Individuals Wollman 2012, Bengston & Jandt 2014, Jandt & al.
within a group can differ in their behavior, and groups, 2014).
© 2021 The Author(s). Open access, licensed under CC BY 4.0
https://creativecommons.org/licenses/by/4.0Social insects provide a unique system in which to
Underlying mechanisms: causes of colony
examine personalities at the group level because of the
personality
multilevel organization of these societies. While indi-
vidual workers can differ from one another in their be- Many mechanisms underlie the emergence of consist-
havior, be it the tasks they tend to perform, the way in ent differences in behavior. Colony personality emerges
which they perform their tasks, or their reproductive from both the behavioral composition of its workers
role in the colony (Turner 1907, Jeanne 1988), col- (Pinter-Wollman 2012) and from the interaction pat-
onies also differ in their behavior from one another terns of these workers that produce collective behaviors
(Pinter-Wollman 2012). Previous reviews of personal- (Gordon 2010). By affecting the ways in which workers
ity in social insects have distinguished between group- interact with one another, ecological conditions can shape
or colony-level personality and the personality of the the behavioral rules that drive colony personality at differ-
individual workers that compose the group (Jandt & ent timescales (Gordon 2019). To explain why consistent
al. 2014). Here, we focus on reviewing the literature differences in behavior among individuals exist, research-
about colony-level personalities, on which the study of ers have modeled physiological and environmental effects
ants provides unique insights and opportunities for fu- on behavior (Sih & al. 2015). Ants are an excellent study
ture research. Because in most ant species workers are system to test these models because they inhabit a large
sterile, natural selection acts at the level of the colony. range of environments, providing opportunities to com-
Therefore, individual differences among ant colonies pare the drivers of personality across different ecological
provide an opportunity to examine how natural selection conditions.
shapes behavioral differences among groups (Jandt & Group composition: Collective behaviors emerge
Gordon 2016). The vast number of ant species provides from the behavior of the individual workers that make
opportunities for evolutionary comparisons that can up the colony. Workers in a colony differ in their behavior
shed light on the causes and consequences of both indi- (Chapman & al. 2011), in their rate of interactions with
vidual and colony personalities, and the links between nestmates (Pinter-Wollman & al. 2011), in their mor-
them. phology (Oster & Wilson 1978), as well as in other traits.
Here, we review the literature on the underlying These differences can be driven by diverse genotypes
causes and consequences of colony personality. Our (Julian & Fewell 2004, Waddington & al. 2010, Eyer
review is not exhaustive and it emphasizes research & al. 2013), differential gene expression (Page & al. 2018),
conducted since the time a number of major reviews on worker age (Tschinkel 2004, Witte & al. 2010), worker
ant personalities were written (Pinter-Wollman 2012, experience (Langridge & al. 2008), and various develop-
Bengston & Jandt 2014, Jandt & al. 2014) and links mental processes (Weidenmüller & al. 2009, Bengston
this more recent work with research conducted before & Jandt 2014). Differences in group composition can
those reviews were written. We begin by detailing how explain differences in colony behaviors because colonies
behavioral differences among colonies can emerge. We may differ in the mean and / or distribution of the types of
then discuss the ecological consequences of behavioral workers that comprise them, leading to different collective
differences between colonies, both at the population outcomes (Pinter-Wollman 2012). The ways in which
level and across ecological communities. We follow with differences among colonies in behavior might emerge from
an examination of the links between causes and conse- differences between individual workers in behavior have
quences of colony personality by highlighting the ability been reviewed by Pinter-Wollman (2012), Jandt & al.
of ants to construct their own niche through the forma- (2014), and Jandt & Gordon (2016). Recent empirical
tion of nests. The study of niche construction has broad studies on the topic have found that the exploratory behav-
implications for understanding the feedback between ior of Formica fusca workers predicts the rate at which a
behavior and the environment (Odling-Smee & al. 1996, group transports brood (Carere & al. 2018); the average
Laland & al. 1999, Day & al. 2003, Odling-Smee & al. aggression of Linepithema humile workers determines
2013) and between the causes and consequences of an- the response of a group to heterospecific competitors
imal personality. Ants provide a unique opportunity to (Neumann & Pinter-Wollman 2019); and the average
study these links because of their ability to manipulate exploration of L. humile workers explains collective nest
their environment. Following our review of the imme- selection (Hui & Pinter-Wollman 2014). Alternatively,
diate causes and consequences of colony personality, extreme behaviors can have important effects on collective
we examine the evolutionary history of such behavioral outcomes (Modlmeier & al. 2014). For example, nests
differences, providing suggestions for future comparative constructed by groups of Veromessor pergandei composed
work that capitalizes on the diversity of ant species. We of both large and small workers had longer and more con-
end with an example of how the study of colony per- nected tunnels than would be expected according to the
sonality in ants can be applied to identify and control additive contributions of each worker size class (Kwapich
invasive species. Throughout the paper, we suggest top- & al. 2018). Examining how colony personalities emerge
ics for future research and highlight questions that the from the behaviors of the workers that compose the colony
study of colony personality in ants is uniquely poised to can inform the study of how consistent collective behaviors
address. emerge in other social systems.
48Interactions among workers in a colony are necessary Future directions: The diversity of ant behaviors
for the emergence of collective behaviors, including the presents an opportunity to compare regulatory mech-
consistency of these collective behaviors (i.e., colony per- anisms across species that have different natural his-
sonality). Worker interactions regulate a variety of colony tories (Gordon 2019). We propose that comparing the
behaviors including foraging (Detrain & Deneubourg mechanisms that underlie the emergence of collective
2009), nest construction (Theraulaz & al. 1998, 2003), behavior among colonies and species that occupy different
nest relocation (Couzin & Franks 2003, Pratt 2005a), environments can shed light on how colony personalities
and others. However, the way in which interactions, and emerge. Such comparative studies may reveal particular
potential consistency in interactions, or consistency in the environmental conditions or mechanisms of behavioral
mechanisms that regulate interactions, influence colony regulation (or combinations of the two) that are associated
personality remains to be investigated. with the evolution and maintenance of personality.
Environmental effects: Colonies that experience
Ecological consequences of colony personality
different external conditions can exhibit different colony
personalities. In Linepithema humile, colonies that are Consistent differences in behavior among individuals
deprived of sucrose consistently decrease their activity and may influence how they respond to abiotic factors in the
aggression compared with well-fed colonies (Grover & al. environment and how they interact with other species.
2007), and aphid presence decreases colony aggression Consistent behavioral differences among ant colonies
(Choe & Rust 2006). Thus, in L. humile, environmen- may determine their ability to acclimate to changing cli-
tal conditions related to nutrition are associated with matic conditions and dictate how they interact with other
consistent differences in colony behaviors, specifically colonies from their own species, other ant species, and
aggression and activity. Colonies that experience different the broader ecological community, including other an-
environmental conditions can also exhibit different colony imals and plants. The link between ecology and colony
personalities through changes in their relative investment personality is bidirectional because the environment
of worker production. For example, in Pheidole pallidula, can influence colony personality (as discussed above),
colonies that sense the presence of other colonies increase and colony personality can influence the ecological envi-
their relative investment in soldier production, presuma- ronment. We discuss this bidirectionality and potential
bly to account for the increased likelihood of competition ways to study it in the section ‘Causes and consequences
(Passera & al. 1996) and thus may exhibit different per- of colony personality are intertwined’. In this section, we
sonalities from colonies that do not produce extra soldiers. focus on the consequences of colony personality at the
The social environment can have a direct effect on colony population, community, and ecosystem levels to highlight
behaviors; for example, Temnothorax longispinosus host the importance of studying ant colony personalities across
colonies behave more aggressively towards their parasitic ecological scales.
competitor Protomognathus americanus (now Temnotho- Relationship between colony personality and
rax americanus, see Ward & al. 2015) compared with a geographical distribution: Ant colonies can differ
non-parasitic competitor (Pamminger & al. 2011). Finally, consistently in how they respond to the environment. Be-
colonies can differ in how they respond to similar environ- cause ants occupy diverse niches over a wide geographic
mental conditions and exhibit different reaction norms range, they present intriguing opportunities for studying
(Dingemanse & al. 2010). For example, colonies of the the interplay between abiotic factors and animal person-
harvester ant Pogonomyrmex barbatus differ in how they ality. For example, Temnothorax longispinosus colonies
regulate foraging activity in response to temperature and from warm environments are more exploratory and more
humidity (Gordon & al. 2011) and these differences can vigilant while foraging and less aggressive than colonies
emerge from different gene regulation in worker brains from cold sites (Segev & al. 2017). In a closely related spe-
(Friedman & al. 2018). cies, Temnothorax rugatulus, colonies in lower latitudes
Alternatively, in some cases, colonies exhibit consist- – where the climate is warm – exhibit lower levels of ag-
ent differences in behavior but have similar responses to gression compared with colonies from cold sites. However,
changes in the environment. For example, colonies of Ver- in contrast with T. longispinosus, colonies of T. rugatulus
omessor andrei consistently differ in their responsiveness from warm sites have high foraging activity along short
and speed across both foraging and disturbance situations. distances (Bengston & Dornhaus 2014). These examples
However, all colonies increase their foraging speed during suggest that the relationship between colony personality
dry conditions, regardless of how much they differ from and climate can differ between closely related species.
one another in foraging behavior (Pinter-Wollman & al. Thus, ants provide a unique opportunity for comparing
2012). Likewise, colonies of the acorn ant Temnothorax within and across species how colony personalities facil-
curvispinosus all show similar increases in foraging rate itate acclimation to abiotic conditions.
when temperatures increase, despite differences among Relationship between colony personality and
colonies in foraging rates in cold temperatures (MacLean ecological interactions: Consistent differences in
& al. 2017). It would be interesting to determine if certain behavior may drive the outcomes of direct or indirect
environmental features are always more likely to drive intra- and interspecific competition. Furthermore, ant
similarities or differences among colony personalities. colony personality may shape the biotic environment at the
49community level due to the wide range of mutualistic and
antagonistic interactions that ants have with other species.
Population level – intraspecif ic inter-
a c t i o n s . Colony personality can shape intraspecific
interactions when competing over resources, such as ter-
ritory and food. The ability to acquire and defend a nest
can influence population density, leading to both direct
and indirect competitive interactions among colonies. In
Temnothorax longispinosus, colonies made up of mostly
aggressive workers are better at defending their nest than
colonies of the same size that consist of mostly non-aggres-
sive individuals (Modlmeier & al. 2014). Furthermore,
intraspecific competition can change colony behavior.
Temnothorax longispinosus colonies that interact with
a conspecific competitor increase their exploration of a
novel environment (Modlmeier & al. 2012). Similarly,
Linepithema humile colonies that regularly encounter
other colonies are more aggressive than isolated colonies
(Thomas & al. 2005). Future work could untangle the
relationship between the causes and consequences of Fig. 1: Difference in colony personality within and between
population density on colony personality. species for contemporaneous colonies. Hypothetical frequencies
Colony personality can influence foraging strategies, of a colony personality trait (e.g., collective aggression) of four
which may have consequences for intraspecific compe- ant species. Each species is depicted in a different color. Symbols
tition. The foraging success of Aphaenogaster senilis on the distribution of the yellow species represent different col-
colonies increases with colony aggression and exploratory ony personalities. The yellow species may face higher levels of
tendencies. However, increased colony aggression and interspecific competition than the other species because colony
exploration leads to increased worker mortality because personalities of this species overlap with colony personalities
workers will forage at temperatures that are too high from other species (e.g., colony personalities represented by
for their physiology (Blight & al. 2016). Thus, the col- the square and triangle). However, the yellow species may be
ony-level advantage of aggressive-exploratory colonies able to withstand competition because it occupies a wider range
(i.e., the positive relationship between foraging and colony of colony personalities than the other species, such as the red
personality) comes at a cost to the individual workers. one, which has a very narrow range of colony personalities.
Solenopsis invicta colonies exhibit consistent differences For example, colonies with the square or circle personalities
in foraging-related behaviors, including outside activity, might be the most successful when the yellow and red species
recruitment, and exploration (Bockoven & al. 2015). High are competing. Colonies with personalities represented by the
activity levels are associated with slow colony growth, triangle or circle would fare better when competing with the
suggesting that consistent differences in foraging-related purple and teal species. If all species are present, it is possible
behaviors may have consequences for colony fitness. Fur- that over time, competition will narrow the colony personality
ther work could compare the direct competition between distribution of the yellow species, leading to an increase in the
colonies that exhibit different foraging behaviors and number of colonies exhibiting the circle personality and elim-
different personality traits to uncover the links between inating those with the square or triangle colony personalities.
colony personality, foraging strategies, and colony fitness. See Figure 2 for detailed hypotheses regarding changes in the
Community level – interspecific in- frequency of colony personalities over time.
t e r a c t i o n s . Interspecific interactions, which can be
mediated by personality traits, influence communities
by shaping species distribution, resource availability, The distribution of colony personalities within a species
and ecosystem services. Competing species may be more can influence competitive interactions, just as the distri-
likely to coexist if populations contain individuals with butions of other attributes shape interspecific interactions
different personalities (Wolf & Weissing 2012). Further- and lead to niche partitioning (Hairston & al. 1960, Con-
more, competition may influence the adaptive value of nell & Orias 1964). Ant species can differ in their ability
different behaviors in different environments (Webster to compete over and defend food and shelter (Buczkowski
& al. 2009). Studying the personality of ant colonies pro- & Bennett 2008, Vonshak & al. 2012). However, the effect
vides an opportunity to uncover the relationship between of colony personality on interactions among different ant
personality and interspecific competition in a diverse species has not been explored extensively. Differences in
clade that occupies a wide range of ecosystems. Here, we competitive ability among colonies within a species may
discuss the effect of colony personality on interactions lead to different competitive outcomes when colonies in
among ant species and interactions between ants and other the extremes of the behavioral distribution of two species
organisms. interact compared with interactions between colonies that
50colony personalities exhibited by M. ebeninus (similar to
Species 1 the red species in Fig. 1) (Saar & al. 2018). Uncovering the
Species 2
bidirectional relationship between interspecific interac-
tions and the distribution of colony personalities within
a species addresses both the causes and consequences of
colony-level personality.
Social parasitism provides a fruitful opportunity for
Personality
examining the effects of colony personality on interspecific
interactions. Social parasitism occurs when one ant species
relies on a host species for some service, such as brood
care, food, or defense (Buschinger 2009, de la Mora
& al. 2020). The personalities of both host and parasite
colonies may influence the interspecific relationship and
the coevolutionary arms race between the species. For
example, host colonies of Temnothorax longispinosus
A B C increase their aggression when exposed to the parasitic
Time 1 Time 2 Time 1 Time 2 Time 1 Time 2 Protomognathus americanus (see Pamminger & al. 2011).
Fig. 2: Changes over time in the colony personality distribution Colonies that exhibit high levels of aggression lose fewer
of competing species. Three hypothetical scenarios of changes brood to parasitizing colonies than colonies that exhibit
in the distributions of colony personalities when two sympatric low aggression, suggesting that colony personality may
species interact (Species 1 and 2). Each species is represented influence the fitness of the hosts (Kleeberg & al. 2014).
by a different color and each panel shows the potential change Interestingly, the rearing conditions of the host species
in colony personality distribution over time. At Time 1, the two can further influence colony personalities. In another
species have similar distributions of colony personalities with study of T. longispinosus and P. americanus, host colonies
some overlap (see distributions of the purple and teal species raised by parasitic workers were faster at finding nest sites
in Fig. 1). If we assume that colonies with similar personalities than host colonies raised by their own workers (Keiser &
from different species compete with each other, we might ex- al. 2015). The study of colony personality can aid in un-
pect that over time there will be a change in the distribution derstanding the evolutionary dynamics of parasite-host
but not in the mean of colony personalities (A) or a change in relationships by focusing on the costs and benefits to both
the mean but not in the distribution (B). These two outcomes host and parasite colonies that differ in their personalities.
are not mutually exclusive and both the mean and distribution Furthermore, comparing the personalities of host colonies
of colony personalities can change over time (C). Differences in ranges where social parasites have not spread with the
between the species at Time 2 might be smaller empirically, and personalities of parasitized colonies could address hypoth-
are intentionally exaggerated in this hypothetical scenario to eses about the role of social parasitism in the development
emphasize the divergence of colony personality distributions. of colony personality in host species.
Interspecific interactions between ants and other or-
ganisms, which shape the structure of ecological com-
are close to the mean of each species (Fig. 1). Furthermore, munities, can be influenced by the personalities of ant
it is possible that species with a greater diversity of colony colonies. Ants can act as mutualists or parasites of plants,
personalities will be more successful than species with a and colony personality may influence these ant-plant
narrower colony personality repertoire because they will interactions. The personality of predatory species can
be able to occupy a larger ecological niche or exhibit more change the community structure of prey species (Wolf
strategies for competition (Fig. 1). We suggest that inves- & Weissing 2012). Furthermore, a variety of parasitic
tigating the effects of colony personality on interspecific microorganisms infect ants, and these associations may
interactions can result in important insights about the interact with colony personality.
composition of ant communities in different regions. Ant-plant interactions may be shaped by colony per-
Further work could identify how the distribution of col- sonality. For example, colony personality can influence the
ony personalities of one species influences the distribution fitness of host plants. Highly aggressive Azteca colonies
of colony personalities of a heterospecific competitor over defend their host plants from herbivores (Pringle & al.
time (Fig. 2). Colonies of Camponotus rufipes that overlap 2011, Marting & al. 2018). However, colony aggression
with a heterospecific competitor Camponotus sericeiven- can deter pollinators from their host plants, as happens
tris exhibit higher levels of aggression than colonies in to plants that host aggressive Solenopsis xyloni colonies
areas without C. sericeiventris (see Espírito Santo & (Ness 2006). Future work can capitalize on systems of
al. 2012). Furthermore, differences in colony personality facultative ant-plant mutualisms (Apple & Feener 2001,
drive coexistence between colonies of Messor arenarius Rudgers 2004) by comparing the personalities of colonies
and Messor ebeninus. Messor arenarius colonies exhibit which live on plants with those that do not, to determine
a large range of colony personalities (similar to the yellow if mutualist colonies are, for example, bolder or more ag-
species in Fig. 1), compared with the narrower range of gressive than colonies without a host plant.
51Personality influences predator-prey interactions in a ality of early and late settling colonies following a major
number of taxa, including birds (Quinn & al. 2012), fish disturbance.
(Jones & Godin 2010), and mammals (Mella & al. 2015). Changes to the environment and changes in behavior
However, these interactions have received less attention in can occur at different timescales. These temporal dif-
studies of social insects. Colony personality may influence ferences can lead to a time lag between environmental
colony defense from predators. Highly aggressive colonies changes and behavioral responses. For example, if an en-
of the harvester ant Pogonomyrmex occidentalis are less vironmental change is rapid (e.g., a severe storm), behav-
likely than low-aggression colonies to have predators ioral rigidity associated with personality might not allow
damage their nests (Wiernasz & al. 2014). It would be animals to respond to the environmental change. Colony
interesting to determine if trade-offs with other colony personalities that rely on the exchange of information
functions, such as brood care or foraging, lead low-ag- about the environment among workers that are spread
gression colonies to be more successful than aggressive out in space (e.g., during foraging or nest relocation) may
colonies in areas with low predation rates. be especially impacted by the time lag between changes
Harmful microorganisms are key players in ecological in the environment and changes to colony personality.
systems, and their interactions, with ants may be impacted Colonies of the harvester ant Pogonomyrmex barbatus
by colony personality. Small colonies of Myrmica rubra ex- differ in how they regulate their foraging behavior in
hibit distinct hygienic behavior that is not seen in large col- response to weather conditions, and these differences are
onies. When infected with a pathogen, these small colonies heritable (Gordon 2013). Because of the long generation
remove brood from the nest, sanitize the interior, and then time of harvester ants, population-level changes to herit-
move brood back into the nest (Leclerc & Detrain 2018). able colony-specific foraging strategies might take longer
In Temnothorax nylanderi, colonies differ in the rate at than changes to the weather caused by human induced
which they remove infected corpses from nests (Scharf climate change. Timescale differences between behavioral
& al. 2012). Thus, it is possible that colonies with different and environmental changes are pertinent when examining
personality traits that are related to hygienic behavior changes to nest structure, which we discuss in detail in
differ in their spread of pathogens throughout the colony. the following section.
Future directions: The study of ant colony personal-
Causes and consequences of colony personality
ity can advance our understanding of trophic interactions
are intertwined
that form food webs. Because colony personalities can
influence foraging strategies and predator-prey dynam- The causes and consequences of animal personality are
ics, and ant species occupy a wide range of trophic levels, intertwined. Ants provide a unique opportunity for exam-
colony personality could have cascading effects across ining the connections between causes and consequences
food webs (Kalinkat 2014). For example, aggressive of personality because many ant species shape their own
Linepithema humile colonies displace Pogonomyrmex niche by constructing nests or relocating between nest
and Veromessor harvester ant species, negatively impact- sites. Colony personality can impact the structures that
ing horned lizards that prey upon these harvester ants ants occupy (e.g., through the excavation of a nest or
(Suarez & al. 2000). Army ants are interesting species through the decision about which nest to move into).
for future studies on food webs and colony personality. Furthermore, nest structures can shape colony behav-
For example, colonies of the army ant Eciton burchellii ior because of the physical constraints that nests im-
can consume tens of thousands of prey items, from a pose on worker interactions (Pinter-Wollman 2015b,
variety of species, in a single day (Franks & Fletcher Pinter-Wollman & al. 2017, 2018). Nests are diverse
1983). Thus, if there are consistent differences among in structure (Tschinkel 2015), ranging in size from the
colonies in their foraging behavior, they may also differ in inside of an acorn (Varoudis & al. 2018) to thousands of
their effects on the environment, and the distribution of connected chambers up to seven meters deep (Moreira
colony personalities could influence the entire ecological & al. 2004). The large diversity of nest structures can
community. facilitate exploration of the relationship between colony
Ecological succession plays an important role in com- personality and constructed niches across different eco-
munity assembly. However, despite the importance of logical contexts and evolutionary histories.
animal personality in determining the outcomes of species Nest construction and excavation: Colonies differ
interactions, few studies have considered the role of per- in the nests they build and live in. Casts and reconstruc-
sonality in ecological succession. For example, it is possible tions of nests from different colonies of the same species
that certain personality traits fare better at different stages have different numbers of chambers (Tschinkel 2004,
of succession. One might expect colonies with high levels 2005, Verza & al. 2007, Guimarães & al. 2018), reach
of exploration to establish early and less exploratory col- different depths (Kleineidam & Roces 2000, Tschinkel
onies to settle later (Fellers 1987, Fogarty & al. 2011). 2004, 2005, Guimarães & al. 2018), and differ in the
Chapple & al. (2012) provide a framework for examining connectivity of the chambers (Pinter-Wollman 2015a).
the effect of personality on biological invasions, which Colonies can differ in the number of nests they occupy,
might be applied to the study of ecological succession as seen in the facultatively polydomous Formica rufa see
more broadly. Future studies could compare the person- (Ellis & Robinson 2014). Among colonies, differences in
52nest structure can be consistent over time. For example, Studying how colonies collectively choose which nests
when colonies of Temnothorax rugatulus were forced to to relocate into can uncover how different processes may
construct a new nest four times over 12 days, some colonies lead to consistent differences in nest site preferences.
tended to build wide walls while others built thin walls For example, among-colony differences in nest prefer-
(DiRienzo & Dornhaus 2017). ence may emerge from differences in the quorum size
The differences among colonies in nest structure could that colonies require to transition from tandem running
emerge from differences in how nests are constructed. The to active transport, as has been studied extensively in
process of nest construction is driven by individual-based Temnothorax ants (Pratt 2005a, b, Pratt & Sumpter
local rules including stigmergy and the use of local tem- 2006). In Myrmecina nipponica, colonies use pheromone
plates (Theraulaz & al. 1998, 2003, Theraulaz 2014, trails to navigate and recruit individuals to a new nest site
Khuong & al. 2016, Bruce & al. 2019, Invernizzi & Rux- until reaching a quorum threshold to start active transport
ton 2019). Species differ in the cues that workers follow of workers and brood (Cronin 2013).
when constructing a nest. For example, Lasius niger work- The decisions whether to relocate, and which nest
ers use feedback to regulate soil deposition and use body site to move into, may be influenced by environmental
size as a template to determine the height and location of a features. These environmental effects on nest relocation
chamber (Khuong & al. 2016). Species of leaf cutter ants, can be studied by comparing colonies within and among
such as Acromyrmex lundi and Atta colombica, cue on the species that occupy similar, or different, environments.
density of workers to initiate digging behavior (Römer & For example, in populations of the harvester ant Pogon-
Roces 2014, Bruce & al. 2019). Differences among colo- omyrmex barbatus, 20% of colonies attempt to relocate
nies in the rules that workers follow when constructing every year but only 10% successfully move (Gordon 1992).
nests, or differences among workers in the templates they It would be interesting to determine what causes only half
use (e.g., due to polymorphism) can lead to differences in of the colonies to relocate successfully. Perhaps there are
the structures that colonies live in (Kwapich & al. 2018). micro-climatic features or certain traits that facilitate
The nest, as an extended phenotype, can shape the the relocation success of some colonies but not others. In
collective behavior of colonies and their personality. Nest contrast with P. barbatus, up to 80% of colonies of the har-
structure can shape differences among colonies in behav- vester ant Veromessor andrei relocate annually (Brown
ior (Pinter-Wollman 2015a, Pinter-Wollman & al. 1999). Veromessor andrei live in serpentine grasslands
2017). For example, nest architecture can shape patterns (Hobbs 1985, Brown 1999) which have different soils from
of worker interactions (Pinter-Wollman 2015b), which where P. barbatus dig their nests. Thus, it is possible that
underlie collective behavior. Indeed, the foraging behavior soil structure leads to differences in relocation frequency
of Veromessor andrei harvester ant colonies is influenced among species and local differences in soil structure could
by the structure of their nests (Pinter-Wollman 2015a). drive differences among colonies of the same species in
The collective behavior of these colonies is consistent as nest relocation behavior. Studying such environmental
long as they remain in a particular nest site (and can there- effects on relocation behavior can expand our understand-
fore be considered a colony personality) but their behavior ing of the feedback between the environment and colony
changes when they move to a new nest (Pinter-Wollman personality.
& al. 2012). Because nests can shape colony behavior and Future directions: The ability of ants to construct
the behavior of the colony (e.g., excavation or relocation) the niches they live in provides an intriguing opportunity
can shape the structure of the nest, ants provide a unique to study the feedback between the environment and per-
opportunity to examine feedback between animal person- sonality. Colony personality may affect how frequently
ality and the environment. colonies relocate among nests or how they construct the
Nest relocation: One form of niche construction is nests they live in. In addition, the nests that colonies con-
relocating into a new nest. Colonies can move regularly struct or choose to relocate into may impact colony person-
among a set of nests (McGlynn 2007), in response to a ality because nest structure influences worker interaction
destruction of their nest (Möglich 1978), to avoid inter- patterns (Burd & al. 2010, Pinter-Wollman & al. 2013,
actions with conspecifics (Brown 1999), or when scouts Pinter-Wollman 2015b). These interaction patterns
encounter high quality nests (Dornhaus & al. 2004). determine collective behaviors, including the collective
Within and between populations, colonies can differ in decision-making process during nest relocation and poten-
how frequently they relocate among nests (Pinter-Woll- tially the decisions made during nest construction. Thus,
man & Brown 2015). These relocations place colonies in ants provide a study system in which multiple components
different nest structures, which, as discussed in the pre- can be manipulated to investigate the feedback between
vious section, can shape colony personality. In addition, nest structure and collective behaviors and / or colony
colonies may differ consistently in how frequently they personalities, and more broadly, the built environment
relocate among nests and these differences may be affected and collective outcomes (Pinter-Wollman & al. 2018).
by other colony behaviors. For example, in Temnothorax Differences among colonies and species in how they
nylanderi, there is a negative relationship between colony construct their nests or how frequently they relocate nests
aggression and the likelihood to relocate into a new nest could emerge from differences in environmental stability.
(Scharf & al. 2012). If colonies modify their behaviors in response to changes
53in the environment, then we may expect colonies that live If evolution favors a high degree of behavioral diversity in
in stable environments to have different nest construction species with a large distribution range, we would expect
and relocation patterns than colonies that live in unstable different species that occupy large ranges to exhibit similar
environments. For example, in unstable environments, levels of behavioral diversity compared with species which
colonies might change the structure of their nests over occupy small ranges. If, however, phylogenetic similarity
time in response to changes in the environment (e.g., is a better predictor of behavioral diversity than distribu-
colonies that live in rainy environments may modify nests tion range size, we might expect closely related species to
more frequently to repair damage caused by rains). Future exhibit a similar degree of behavioral diversity, regardless
research could explore how differences in the timescale of the geographical range and environments they each
over which collective behaviors change and the environ- occupy. For example, Temnothorax longispinosus (see
ment changes affect the feedback between the two and Segev & al. 2017) and Temnothorax rugatulus (see Beng-
shape colony personalities. Because ants live in a range ston & Dornhaus 2014) are closely related species that
of environments that differ in stability and because they exhibit similar amounts of differences among colonies in
can shape their local environment, they are a powerful personality, despite having differently sized geographic
system in which to study the feedback between consistent ranges. Thus, it is possible that the shared phylogenetic
differences in behavior and environmental changes, which history of these two species provides a better explanation
can occur at different timescales. for their similarities in behavioral diversity than the size
of their geographical range.
Evolution of colony personality
Comparisons among species can help determine the
Ants provide a unique opportunity to examine the evo- causes that underlie the emergence of personality and
lutionary trajectory of animal personalities. While some disentangle heritable components from developmental
theory has investigated possible explanations for how causes. In some species, personality may be driven pre-
personalities have evolved (Wolf & Weissing 2010, Sih dominantly by genetic effects, whereas in others it may
& al. 2015), empirical evidence is still lacking. The com- emerge primarily from ontogenetic effects. Comparing
parative approach is one of the primary ways to study the species can reveal which ecological conditions might favor
evolution of behavior because behavior typically does genetic or developmental drivers for colony personality.
not leave a fossil record (Hsieh & Plotnick 2020). The For example, in Pogonomyrmex barbatus, younger colo-
diversity of ants, with more than 12,000 identified species nies are more aggressive towards conspecifics than older
(Hölldobler & Wilson 1990), can facilitate comparative colonies (Gordon 1991, 1995). In contrast, Temnothorax
investigation of the evolution of colony personality. By rugatulus colonies do not show a relationship between age
comparing across species that have similar or different and aggression (Bengston & Dornhaus 2014). Instead,
life history traits, ecological roles, and environmental colonies that grow faster and invest more in reproductives
constraints, we can uncover sources of differences among (queens and males) are more aggressive compared with
colonies. When conducting comparative analyses (e.g., colonies that grow slower and invest more in sterile work-
meta-analyses), one must consider the literature that is ers (Bengston & al. 2017). Thus, the drivers and presence
sampled, as some questions have received more atten- of consistent individual differences between colonies likely
tion than others. It is further important to be cautious differ between these two species: In P. barbatus, colony
when choosing which data to compare because there aggressive behavior is plastic and changes over develop-
might be differences in how behaviors are measured and ment, whereas in T. rugatulus, colony aggressive behavior
reported. is stable over a lifetime and therefore might have stronger
Sources of differences between colonies: Within genetic drivers than in P. barbatus, forming a life-long
a species, colonies may differ in the selection pressures colony personality. Such comparisons among species of
they experience, with species that have larger distribution ants might uncover novel sources of consistent differences
ranges often experiencing greater differences among colo- among colonies in behavior.
nies and species with smaller ranges potentially experienc-
Application of the study of ant colony
ing more uniform pressures. Species’ distribution can help
personalities
explain the evolution and maintenance of different colony
personality types as well as the amount of behavioral di- Colony personality can mediate the ways in which ants
versity across individuals and populations. Depending on interact with their environment, as detailed in previous
which colony personality is examined, it can be quantified sections. The invasion by ants into novel ecosystems rep-
as either a continuous or a discrete trait. Comparing the resents an important link between colony behavior and the
degree to which colonies differ in their personality across environment (McGlynn 1999, Tsutsui & Suarez 2003,
different species, which occupy different geographical Weis & Sol 2016). Invasive ants are a concern across eco-
ranges and environments, may help uncover the relation- systems globally because they displace native species and
ship between species distribution, evolutionary pressures, disrupt ecological communities (McGlynn 1999, Holway
and personality. For example, one could compare differ- & al. 2002, Bos & al. 2008). Although many ant species
ences in colony personalities among related or unrelated have the opportunity to invade new habitats, only a frac-
species that have different or similar distribution ranges. tion of them successfully establish and persist (Suarez &
54Underlying Colony Ecological
mechanisms personality traits consequences
Aggression
Geographical
Group Exploration distribution
composition
Boldness Population-level
Environmental interactions
Activity level
effects Community level
Hygienic behavior interactions
Niche construction
Fig. 3: Summary of the relationships between the causes and consequences of colony personality that we identified in our review.
Solid arrows are links that we discussed in the review. Dashed orange lines are a few of the many relationships we propose would
be interesting topics for future research.
al. 2005). Ten genera and at least 150 species of ants have seasonality, affect colony personality, because there can
invaded native ecosystems (Holway & al. 2002, Cremer be differences in the traits that characterize invasive spe-
& al. 2008), making ants a good system for the study of cies in non-native populations based on access to certain
personality and conservation biology. foods.
Characteristics of invasive species: Invasive Colony personality and conservation biology:
ant species may share colony-level traits, including cer- Ants provide an opportunity to study the effects of per-
tain collective behaviors that allow them to successfully sonality on invasion risk. While current invasion biology
expand into new ranges. These traits include flexibility research has begun to uncover the impacts of invasions,
in nesting behavior and dietary requirements, polygyny how personality influences the probability of successful
(multiple queens), colony reproduction by budding, and colonization by invasive species is not well known. The
reduced intraspecific aggression (McGlynn 1999, Hol- study of ant colony personality can benefit the field of
way & al. 2002, Tsutsui & Suarez 2003). Furthermore, conservation biology by providing information on key
invasive populations express different collective behav- characteristics of invasive species. For example, Linepi-
iors from those observed in native populations (Suarez thema humile workers are attracted to water in urban
& al. 1999, Holway & al. 2002). For example, in Europe, areas (Holway & Suarez 2006, Fitzgerald & al. 2012,
invasive colonies of Linepithema humile explore novel Fitzgerald & Gordon 2012). If there are individual dif-
environments and detect food resources more quickly ferences among colonies (in the native or invaded range) in
than their native counterparts (Blight & al. 2017). Sim- their reliance on water, this information could prove useful
ilarly, colonies of L. humile in North America are more for determining which colonies might invade arid regions
aggressive than native colonies, potentially facilitating the and could be used for controlling or preventing invasion.
displacement of native ants in the invaded range (Heller By studying ant colony personality, we can construct risk
2004). However, the mechanisms that underlie the plas- assessments that will help prevent the continued spread of
ticity that facilitates these behavioral differences is likely invasive ants. Furthermore, studying personality can help
the same in introduced and native populations (Felden identify which species have the potential to be invasive
& al. 2018). Invasive colonies of Solenopsis invicta that and if any personality traits are associated with the native
are located far from the initial introduction location of species that withstand invasion. Such a study could help
the species in North America exhibit higher levels of predict which native species will be impacted the most by
exploration and forager recruitment than colonies near the introduction of an invasive species (e.g., Figs. 1 and 2).
the site of introduction (Bockoven 2015). While these Studies of colony personalities can improve our un-
invasive characteristics have been observed in a variety derstanding of how personality affects the stages of an
of ant species, future research may examine how fea- invasion – transport, introduction, establishment, and
tures of the environment, such as food availability or spread. Animal personality can affect introduction success
55because different personality traits might have different Bockoven, A.A. 2015: Causes and consequences of intraspecific
impacts on the different stages of invasions. Furthermore, variation in behavior of the red imported fire ant. – PhD
thesis, Texas A&M University, College Station, TX, XI+125 pp.
species invasion may act as a selective force in the intro-
Bockoven, A.A., Wilder, S.M. & Eubanks, M.D. 2015: In-
duced range – favoring personality traits that promote
traspecific variation among social insect colonies: persistent
invasion success (Chapple & al. 2012). Comparisons of regional and colony-level differences in fire ant foraging
personality traits among species or individuals that are behavior. – Public Library of Science One 10: art. e0133868.
successful at invading new habitats and those that are Bos, M.M., Tylianakis, J.M., Steffan-Dewenter, I. &
not, can inform conservation actions (Wright & al. 2010). Tscharntke, T. 2008: The invasive yellow crazy ant and
Understanding the dynamics of an invasion could provide the decline of forest ant diversity in Indonesian cacao agro-
researchers with insight on how invasive ants are estab- forests. – Biological Invasions 10: 1399-1409.
lished and during which stages of invasion they are most Brown, M.J.F. 1999: Nest relocation and encounters between
vulnerable to management. colonies of the seed-harvesting ant Messor andrei. – Insectes
Sociaux 46: 66-70.
Conclusion Bruce, A.I., Pérez-Escudero, A., Czaczkes, T.J. & Burd,
M. 2019: The digging dynamics of ant tunnels: movement,
In our examination of the literature on ant colony person-
encounters, and nest space. – Insectes Sociaux 66: 119-127.
ality, we identified a range of links between the causes and
Buczkowski, G. & Bennett, G.W. 2008: Aggressive interactions
consequences of colony personality, as well as topics for
between the introduced Argentine ant, Linepithema humile
future investigation (Fig. 3). We highlight future research and the native odorous house ant, Tapinoma sessile. – Bio-
efforts that could be addressed uniquely through studies logical Invasions 10: 1001-1011.
on ants. The diversity of ant species opens up countless Burd, M., Shiwakoti, N., Sarvi, M. & Rose, G. 2010: Nest ar-
opportunities for examining the underlying causes and chitecture and traffic flow: large potential effects from small
ecological consequences of personality at multiple scales. structural features. – Ecological Entomology 35: 464-468.
The diversity of ants leaves many unexplored species and Buschinger, A. 2009: Social parasitism among ants: a review
ecological systems and provides ample opportunities for (Hymenoptera: Formicidae). – Myrmecological News 12:
comparative work. Ants provide a unique system in which 219-235.
to study the feedback between causes and consequences of Carere, C., Audebrand, C., Rödel, H.G. & d’Ettorre, P.
personality because of their ability to modify the environ- 2018: Individual behavioural type and group performance in
Formica fusca ants. – Behavioural Processes 157: 402-407.
ment in which they live. We believe that future work on ant
colony personality will benefit the broad field of animal per- Chapman, B.B., Thain, H., Coughlin, J. & Hughes, W.O.H.
2011: Behavioural syndromes at multiple scales in Myrmica
sonality by capitalizing on the exceptional features of ants.
ants. – Animal Behaviour 82: 391-397.
Acknowledgments Chapple, D.G., Simmonds, S.M. & Wong, B.B.M. 2012: Can
behavioral and personality traits influence the success of
We thank Julie Miller, Natalie Lemanski, Gabriella Najm, unintentional species introductions? – Trends in Ecology &
Nitika Sharma, Amanda Klingler, and Alejandra Gam- Evolution 27: 57-64.
boa for their suggestions during the preparation of this Choe, D.-H. & Rust, M.K. 2006: Homopteran chemical signa-
manuscript. tures reduce aggression of tending ants. – Chemoecology
16: 175-178.
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