Ant Thermal Tolerance: A Review of Methods, Hypotheses, and Sources of Variation - Oxford Academic Journals
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Annals of the Entomological Society of America, 114(4), 2021, 459–469
doi: 10.1093/aesa/saab018
Advance Access Publication Date: 11 May 2021
Review
Review
Ant Thermal Tolerance: A Review of Methods, Hypotheses,
and Sources of Variation
Karl A. Roeder,1,4, Diane V. Roeder,2 and Jelena Bujan3
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1
USDA, Agricultural Research Service, North Central Agricultural Research Laboratory, Brookings, SD 57006, USA,
2
Department of Evolution, Ecology, and Behavior, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA,
3
Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland, and 4Corresponding author, e-mail: karl.
roeder@usda.gov
Subject Editor: Gadi V. P. Reddy
Received 17 February 2021; Editorial decision 12 April 2021
Abstract
Ants (Hymenoptera: Formicidae) are a conspicuous group of ectotherms whose behavior, distribution, physi-
ology, and fitness are regulated by temperature. Consequently, interest in traits like thermal tolerance that en-
able ants to survive and thrive in variable climates has increased exponentially over the past few decades. Here,
we synthesize the published literature on the thermal tolerance of ants. We begin our review with discussion of
common metrics: critical thermal limits, lethal thermal limits, knock-down resistance, chill-coma recovery, and
supercooling. In particular, we highlight the ways each thermal metric is quantified and offer a set of methodo-
logical caveats for consideration. We next describe patterns and hypotheses for ant thermal tolerance along
spatial and temporal temperature gradients. Spatially, we focus on relationships with latitude, elevation, ur-
banization, and microclimate. Temporally, we focus on seasonal plasticity, daily variation, dominance-thermal
tolerance tradeoffs, and acclimation. We further discuss other sources of variation including evolutionary his-
tory, body size, age, castes, and nutrition. Finally, we highlight several topics of interest to ant thermal biolo-
gists, ranging in scope from methods development to the impacts of climate change.
Key words: acclimation, Formicidae, temperature, thermal limit, trait
Temperature is one of the key abiotic constraints on ecological com- temperature by increasing leaf transpiration via feeding (Pincebourde
munities and their constituent biological organisms (Chown and and Casas 2019) and darker cuticles from higher levels of melanin in
Nicolson 2004, Angilletta 2009, Sibly et al. 2012). From the frigid ants that enable rapid warming of body temperature in cold envir-
arctic to the sweltering desert, mean annual temperatures can range onments (Bishop et al. 2016). Yet, perhaps one of the most important
over 60°C with yearly, monthly, and daily fluctuations creating en- physiological traits for ectotherms is their thermal tolerance (i.e., the
vironments that are thermally variable across space and through range of temperatures at which an organism can survive). Interest
time (New et al. 1999, Ghalambor et al. 2006, Kearney et al. 2014). in thermal tolerance and how or why it varies across the insect tree
As global temperatures and temperature variability are predicted of life has increased in recent years with large syntheses across mul-
to increase (Parmesan and Yohe 2003, Deutsch et al. 2008, IPCC tiple arthropod groups as well as taxa-specific studies on bees, bee-
2018), understanding how organisms tolerate both the hot and the tles, caddisflies, flies, grasshoppers, mayflies, stoneflies, termites, and
cold climates of our planet remains a fundamental question. true bugs (Klok et al. 2004, Kellermann et al. 2012, Hoffmann et al.
Most animals, including insects, are ectotherms whose physi- 2013, Sheldon and Tewksbury 2014, Oyen et al. 2016, Slatyer et al.
ology—development, metabolism, and reproduction—is constrained 2016, Klockmann et al. 2017, Polato et al. 2018, Janowiecki et al.
by temperature (Harrison et al. 2012, Colinet et al. 2015, Sinclair 2020, Just and Frank 2020). Here, we aim to provide a first review
et al. 2016). Insects must therefore carefully regulate their activity on thermal tolerance of one group—the ants.
in thermally challenging environments and have evolved a number We focus on ants as they are an abundant, diverse, and eco-
of behavioral, morphological, and physiological traits toward logically important group of insects (Hölldobler and Wilson 1990,
improving survival. Examples include aphids reducing microclimate Lach et al. 2010, Economo et al. 2018). Ants are geographically
Published by Oxford University Press on behalf of Entomological Society of America 2021. This work is 459
written by (a) US Government employee(s) and is in the public domain in the US.
460 Annals of the Entomological Society of America, 2021, Vol. 114, No. 4
widespread (Dunn et al. 2009, Jenkins et al. 2011, Gibb et al. 2015) environmental temperatures with activity patterns (Whitford and
and provide numerous ecosystem services such as seed dispersal, Ettershank 1975, Marsh 1988, Cerdá et al. 1998, Villalta et al.
predation, soil aeration, and nutrient cycling (Lobry de Bruyn and 2020). As the field of ant thermal ecology evolves, new techniques
Conacher 1990, Folgarait 1998, Philpott and Armbrecht 2006, Del have been developed to quantify critical thermal limits (Kaspari et al.
Toro et al. 2012). Moreover, a rich history of ant thermal biology 2015), lethal thermal limits (Arnan and Blüthgen 2015), knock-down
exists in the literature with measures of physiological tolerance from resistance (Angilletta et al. 2007), chill-coma recovery (Tonione et al.
Mary Talbot’s seminal work dating back almost 100 yr (Talbot 2020), and supercooling points (Hahn et al. 2008). Consequently,
1934, Talbot 1946). Myrmecologists since then have spent copious methods used to measure the spectrum of thermal traits vary in com-
amounts of time documenting patterns of activity in relation to abi- plexity from simple ramping protocols using dry baths (Bujan et al.
otic variables like temperature and humidity (Kaspari 1993, Perfecto 2020a, Roeder et al. 2021) to more complex molecular techniques
and Vandermeer 1996, Bestlemeyer 2000, Lessard et al. 2009, Stuble for quantifying heat shock protein gene expression (Gehring and
et al. 2013, Prather et al. 2018). Yet, the quantification of physio- Wehner 1995, Ślipiński et al. 2015). The first part of our review
logical traits like thermal tolerance that underlie observed ant explores these methodological differences in how thermal tolerance
activity patterns have only become popular within the last 30 yr has been measured in ants.
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(Cerdá et al. 1998, Meisel 2006, Diamond et al. 2012, Baudier et al.
2015, Kaspari et al. 2015, Bujan et al. 2020a). Critical and Lethal Thermal Limits
We began our review on the topic of ant thermal tolerance by first Dynamic ramping assays using digital thermal dry baths or dry
searching Web of Science using the terms ‘ant’ AND ‘thermal toler- block incubators are currently the most common technique used by
ance’ and expanding that query with Google Scholar by searching researchers to study ant thermal tolerance. In short, individual ants
‘ant*’ OR ‘Formicidae’ AND ‘thermal’ OR ‘heat*’ OR ‘warm*’ OR are placed in small, often 1.5 ml microcentrifuge tubes and checked
‘cold*’ OR ‘cool*’ AND ‘tolerance’. We then supplemented or re- at set time intervals for loss of muscle control or righting response
stricted our literature search in four ways: (1) we scanned publica- (i.e., their critical thermal limits [Huey et al. 1992]). After each
tion records from ant thermal biologists and added relevant papers check, temperature is decreased or increased until all ants in a trial
that had been missed by search engines, (2) we included three pre- reach their critical thermal minimum (CTmin) or maximum (CTmax).
prints from 2020 that contained unpublished work, (3) we included Since 2010, the use of thermal dry baths and dry block incubators
Ph.D. dissertations, MS theses, and undergraduate theses if the work has steadily increased, likely because the equipment is relatively
was unpublished, and (4) we removed papers without a physio- cheap (e.g., ~ $500 for a dry bath), the protocol is straightforward,
logical trait measurement of thermal tolerance. In total, 118 papers and large amounts of data can be rapidly collected. However, there
met our search criteria, 92% of which were published over the past have been important differences in the methodology used by re-
three decades (Fig. 1, Supp Table S1 [online only]). We focus our searchers to measure critical thermal limits. First, the interval time
review on methodological differences and the ecological hypotheses in which ants are subjected to a certain temperature value differs
within these papers with additional discussion on trait variation and across studies with values ranging from 1 to 10 min (Kaspari et al.
why trait variation may occur. 2015, Diamond et al. 2017, Penick et al. 2017). Second, the magni-
tude of temperature change at each time interval transition is often
1°C or 2°C resulting in ramping rates that range from 0.1°C min-1
Methods for Measuring Ant Thermal Tolerance
to 1.0°C min-1 (Baudier et al. 2015, Nowrouzi et al. 2018, Leong
The number of studies measuring ant thermal tolerance exploded et al. 2020). Third, the starting temperature for CTmin assays range
around 1990 as researchers more readily incorporated physio- from 15°C to 26°C and for CTmax from 25°C to 40°C (Wittman et al.
logical traits into ecological studies that had traditionally correlated 2010, Bentley et al. 2016, Bishop et al. 2017). Finally, the material
used to eliminate thermal refugia in the microcentrifuge cap during
thermal tolerance assays has been commonly reported as cotton, but
other materials like modeling clay have been used (Bujan et al. 2016,
Roeder et al. 2018).
As a precursor to digital dry baths, water baths have been used
since 1985 to measure thermal tolerance with ramping or static
assays (Marsh 1985, Jumbam et al. 2008, Chick et al. 2020). For
water bath ramping assays, trials are performed in a similar fashion
to those for thermal dry baths with comparable temperature starting
points and ramping rates (Chown et al. 2009, Warren and Chick
2013, Verble-Pearson et al. 2015, Andrew et al. 2019, Chick et al.
2020). However, the number of ants per container varies between
the two methods with dry bath trials almost always using one in-
dividual per container and water baths using 1 to 18 individuals
per container (Andrew et al. 2013, Boyle et al. 2020). For static
assays, a group of ants is placed in a container at a set tempera-
ture and the number of live ants is recorded after a predetermined
length of time that ranges between 10 and 60 min (Francke et al.
1985, Fitzpatrick et al. 2013, Fitzpatrick et al. 2014). Such trials are
often performed along a temperature array with new batches of ant
Fig. 1. Cumulative and yearly number of published ant thermal tolerance
workers for each temperature to determine the point at which 50%
papers through time. Note: cumulative line and yearly points are on different of workers perish—the lethal temperature or LT50. It is unclear why
scales. there is a current exodus from methods using water baths. We posit
Annals of the Entomological Society of America, 2021, Vol. 114, No. 4 461
that digital dry baths may simply be easier to use with greater tem- between −20°C and −38°C, which is much lower than their CTmin
perature and ramping precision. (Ohyama and Asahina 1972, Berman and Leirikh 2018). Yet super-
Early ant thermal studies also focused on quantifying upper LT50 cooling measurements remain rare for almost all species possibly
values using static assays on hot plates (Cerdá et al. 1997, Cerdá because (1) the methods to measure supercooling points are more
et al. 1998, Cerdá and Retana 2000). In general, between 3 and complicated than those used to measure other lower thermal limits
20 ants would be placed in a container at a set temperature for and (2) the temperature at which supercooling points occur are less
10 min and the number of workers that survived would be recorded. ecologically relevant to many thermal biologists that work in trop-
Temperature would then be increased 1°C or 2°C and the assay ical rainforests and deserts. Nonetheless, supercooling points may
would be repeated with a new set of ants (Cerdá et al. 1998, Oms be of interest for those working in northern latitudes or along eleva-
et al. 2017). Initial temperature starting points for such assays could tional gradients as they more accurately represent a true lower lethal
be as low as 20°C and as high as 50°C (Arnan et al. 2012, Villalta limit that ants may experience (Heinze et al. 1996).
et al. 2020). The use of hot plates to measure LT50s of ants has de-
creased in recent years, but similar methodology is still employed for Caveats and Considerations
both ramping and static assays by investigators using incubators and
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Given the variety of traits and tolerances measured by thermal
environmental chambers (Holway et al. 2002, Jayatilaka et al. 2011, biologists, it should not be surprising that methodological dif-
Wiescher et al. 2011, Asfiya et al. 2016, Yela et al. 2020). ferences occur and that they can have important implications for
interpreting results (Kaspari et al. 2015, Bentley et al. 2016, Leong
Knock-down Resistance and Chill-coma Recovery et al. 2020). We offer a few thoughts. First, thermal tolerance may
Two alternatives to critical and lethal thermal limits are knock-down be plastic across space and through time. We expand upon these
resistance and chill-coma recovery, both of which focus on time and ideas later in this review with examples of intraspecific variation
not temperature as the response variable of interest. Knock-down across populations (Warren and Chick 2013, Chick et al. 2020) and
resistance is the amount of time it takes for an ant to lose mo- across daily fluctuations in temperature (Esch et al. 2017, Nelson
bility at a stressful temperature (Angilletta et al. 2007, Boyles et al. et al. 2018). Here, we simply urge researchers to think about when
2009, Maysov 2014, McGlynn et al. 2020). Environmental cham- to collect ants for thermal assays and then report that time and its
bers, water baths, and thermogradient devices have all been used to associated temperature more regularly in publications. Second, more
measure knock-down resistance, yet literature records of this trait than one colony should be used to calculate mean values for ant
for ants are sparse perhaps because a priori knowledge of critical species as environmental, genetic, nutritional, and other differences
or lethal thermal limits for species are required. Knock-down resist- can occur that affect thermal traits. Third, the amount of time that
ance, however, may represent a more realistic measurement of how ants are kept in captivity may impact physiological traits. For field
long individuals can forage in thermally stressful environments, es- caught ants, thermal assays are generally performed within 2–6 h,
pecially for thermophilic desert ants like Cataglyphis that are active but there is no consistent standard (Oberg et al. 2012, Baudier et al.
at and beyond their thermal limits (Wehner et al. 1992). 2015, Bishop et al. 2017). For lab colonies, ants may be acclimated
Chill-coma recovery is defined as the amount of time required to to or stressed by abiotic conditions and the measured traits of co-
recover from a low temperature in which a chill coma occurs—a tem- horts after multiple generations in the lab may not be comparable
perature that is commonly below the CTmin of a species (Terblanche to wild populations. Fourth, experimental controls should be used
et al. 2011, Sinclair et al. 2015). To induce a chill-coma, environ- and reported with thermal trials. We recommend two: (1) a control
mental chambers or ice baths are often used to create environments group of ants in separate containers that are kept at ambient con-
ranging between −5°C to 0°C in which ants are exposed for 20 to ditions whose survival is monitored regularly during assays and (2)
180 min (Boyles et al. 2009, Tonione et al. 2020). Ants are then secondary verification of experimental chamber temperature with a
moved to arenas around 25°C and time is recorded until movement temperature probe, thermocouple, or thermometer. Finally, variance
begins (Angilletta et al. 2007, Nguyen et al. 2019). To date, chill- in thermal tolerance may occur simply due to differences in experi-
coma recovery studies have primarily focused on cold tolerant spe- mental setup. Large ants with long legs, for example, may escape
cies like Aphaenogaster picea and Prenolepis imparis (Nguyen et al. the thermally limiting boundary layer in experiments with hot plates
2019, Tonione et al. 2020) or invasive species like Myrmica rubra and environmental chambers, but those morphological benefits dis-
and Solenopsis invicta (Boyles et al. 2009, Maysov 2014). Little in- appear in boundary layer-free thermal dry baths.
formation exists for chill-coma recovery times of tropical species be-
yond the leaf cutting Atta sexdens in São Paulo, Brazil (Angilletta
et al. 2007). Ant Thermal Tolerance Across Space
Temperature gradients along latitude, elevation, urbanization, and
Supercooling microclimate represent an array of conditions on which ants can
Supercooling is a phenomenon in which the body tissues and specialize or be limited. We discuss below four spatial patterns in ant
fluids of an individual are maintained in a liquid state below their thermal tolerance and the hypotheses that are frequently tested along
freezing point (Salt 1961, Bale 1987, Sinclair et al. 2003). For these spatial gradients that range in extent from global to local.
freeze-intolerant species, the supercooling point represents a lethal
lower limit where body fluids freeze and ice is formed. Methods to Latitude
measure supercooling points often require attaching a thermocouple As you move from the equator to the poles, environmental temperat-
or temperature probe to the abdomen of an ant and then reducing ures generally cool and become more variable, leading biologists to
the temperature of an experimental setup by 0.1°C min-1 to 10.0°C often hypothesize ways that diversity—be it taxonomic, functional,
min-1 until a small amount of latent heat is released (Cannon and or phylogenetic—changes across latitude (Pianka 1966, Hillebrand
Fell 1992, Hahn et al. 2008). Results from supercooling assays sug- 2004, Mittelbach et al. 2007). In thermal biology, one frequently as-
gest groups like carpenter ants may be able to tolerate temperatures sessed latitudinal pattern is the climate variability hypothesis, which
462 Annals of the Entomological Society of America, 2021, Vol. 114, No. 4
posits that animals from less variable climates (e.g., the tropics) are Urbanization
thermal specialists and have a narrower breadth of thermal tolerance More than four billion people live in urban areas across the globe
compared to their counterparts from seasonal environments (Janzen (United Nations 2019). Projections suggest this number will continue
1967, Stevens 1989, Gaston et al. 2009). There exist few true tests to increase throughout the 21st century as the human population
of the climate variability hypothesis using ants across latitude with grows and people migrate from rural to urban areas. The anthropo-
both support for (Diamond and Chick 2018a) and against (Bujan genic footprint required to harbor this growing population will like-
et al. 2020a) the predicted pattern. wise increase, challenging ectotherms in cities with hotter and more
The thermal adaptation hypothesis similarly predicts that variable temperatures as impervious surface increases and vegetation
thermal limits are locally adapted to environmental temperatures decreases (Memon et al. 2008, Imhoff et al. 2010). One might posit
such that (1) hotter environments are predicted to harbor ants with that the hotter temperatures in urban areas should promote greater
higher thermal tolerance and (2) thermally variable environments heat tolerance which, at least at an intraspecific level, has been docu-
generate organisms with broad thermal ranges (Kaspari et al. 2015, mented in Aphaenogaster spp. (Warren et al. 2018), Atta sexdens
Kaspari et al. 2016). Evidence for thermal adaptation does exist for (Angilletta et al. 2007), Temnothorax curvispinosus (Diamond et al.
ants with CTmin and CTmax being correlated with the temperature 2017), and Wasmannia auropunctata (Foucaud et al. 2013). In add-
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of the environment (Diamond and Chick 2018b), plus species from ition to higher heat tolerance, urban Temnothorax populations can
low latitudes are often more heat tolerant (Diamond et al. 2012). also tolerate rapid warming better than rural populations, likely
Intraspecific differences in ant thermal tolerance, while rarely exam- representing an adaptation to high temperature fluctuations in cities
ined across latitude, also suggest adaptation in cold tolerance can (Diamond et al. 2018a). Ant cold tolerance, however, does not al-
occur across populations of Aphaenogaster picea and Wasmannia ways co-vary with urbanization (Angilletta et al. 2007, Diamond
auropunctata near the edge, compared to the center, of their geo- et al. 2017, Warren et al. 2018). Patterns for hot and cold tolerance
graphic distribution (Rey et al. 2012, Nguyen et al. 2019). But evi- are mixed, but perhaps this result should not be surprising given the
dence for thermal adaptation has been mixed as temperature alone selective pressure by hot urban temperatures on upper and not lower
was a poor predictor of heat tolerance for ants in North America thermal limits.
(Bujan et al. 2020a). Considering that the number of described ant There is clear interest in differences of thermal traits between
species is ~15,000 (www.antcat.org, Economo et al. 2018), it may be urban and rural ant populations, yet we still know little about
difficult to fully test macroecological hypotheses until global data- underlying mechanisms for why disparities occur. Common garden
bases are expanded to include more species from other geographic experiments primarily advocate for adaptive evolution (Diamond
regions. et al. 2017; Diamond et al. 2018a, b; Martin et al. 2019), although
acclimatization is not conclusively excluded. Alternatively, differ-
Elevation ences in thermal tolerance have been hypothesized to arise via se-
lection, drift, or bottleneck effects (Foucaud et al. 2013). Once ant
Increases in altitude generally coincide with lower temperatures,
colonies have been established, for example, gene flow may be min-
resulting in different selective pressures on ectotherm thermal tol-
imal between urban and rural populations due to warmer temperat-
erance across elevational gradients (e.g., cold tolerance at high eleva-
ures advancing reproductive phenology and creating asynchronous
tions and heat tolerance at low elevations). Indeed, species are more
mating events (Chick et al. 2019). This effect may intensify along
cold tolerant at higher elevations in South African ant communities
other gradients (e.g., latitude, elevation), minimizing the chance of
(Bishop et al. 2017) and within the doryline army ants of Costa Rica
gene exchange and driving differences in thermal tolerance between
(Baudier et al. 2018). Populations of Aphaenogaster picea, Eciton
populations.
burchellii, Prenolepis imparis, and Solenopsis invicta are likewise
more cold tolerant (i.e., lower CTmin) at high compared to low eleva-
tions (Warren and Chick 2013, Baudier and O’Donnell 2018, Lytle Microclimate
et al. 2020, Tonione et al. 2020). However, the relationship between While we have primarily focused on global or regional gradients,
heat tolerance and elevation is less predictable (Baudier et al. 2015, temperature can also be extremely heterogeneous within a site that
Bishop et al. 2017, Baudier and O’Donnell 2018, Nowrouzi et al. is experiencing the same macroscale climate conditions (Potter
2018, Villalta et al. 2020, Yela et al. 2020) and may be harder to et al. 2013, Kearney et al. 2014). The aptly named microclimate
generalize across elevational gradients if temperatures are not se- is thought by many to be more important for organisms like ants
vere enough to impose selective pressure. Thus, ant communities as it represents the localized abiotic conditions that individuals ac-
and individual species along elevational gradients tend to support tually experience (Kaspari 1993, Perfecto and Vandermeer 1996,
Brett’s rule (Brett 1956)—a third macroecological hypothesis that Bestelmeyer 2000). Consequently, microclimate may help account
posits less geographic variation occurs in heat tolerance than in cold for some of the variation in patterns of ant diversity within a site as
tolerance. species with different heat and cold tolerance values operate in dif-
We caution relying completely on past results from hypoth- ferent habitats. In a Mediterranean community, for example, open
esis tests as species distributions will undoubtedly shift during cli- and shaded habitat types significantly predicted ant heat tolerance
mate warming. Invasive ants, in particular, will begin to move ‘up (Arnan and Blüthgen 2015). And even in the climatically stable
the mountain’ and encroach on native ant species that once sought tropics, microclimatic changes caused by deforestation impacted
refuge in the cold temperatures of higher elevations. For example, functional activity of ant genera (Boyle et al. 2020) and foraging
Aphaenogaster picea can tolerate low temperatures and inhabit high patterns of army ants such that above-ground species reduced their
elevations, a barrier that is currently limiting the upward invasion foraging activity in hot open areas (Kumar and O’Donnell 2009).
of Brachyponera chinensis and Solenopsis invicta (Lytle et al. 2020, Vertical stratification of temperature can also occur between the
Warren et al. 2020). However, this refuge is likely only temporary as soil and canopy. Canopies are on average hotter and more variable
heat tolerant ants continue to track up mountain slopes and replace with ant species that have higher heat tolerance compared to their
more heat intolerant species (Warren et al. 2016). litter counterparts (Kaspari et al. 2015, Bujan et al. 2016), while soil
Annals of the Entomological Society of America, 2021, Vol. 114, No. 4 463
buffers temperature changes and supports subterranean ants with Daily
lower thermal tolerances (Baudier et al. 2015). Temperature can fluctuate over 30°C during a daily cycle, creating
and limiting opportunities for ants to be active as the ground warms
via solar heating. Perhaps unsurprisingly, thermal tolerance values
Ant Thermal Tolerance Through Time vary among species that operate along this daily temperature gra-
Temporal differences in thermal conditions play a critical role in dient. Diurnal ants like Myrmecia croslandi have higher CTmin and
structuring ant communities as species and individuals may be CTmax than their sympatric congener, Myrmecia pyriformis, whose
thermally adapted to, or adjust their behavior in response to, dif- activity is limited to cooler nocturnal hours (Jayatilaka et al. 2011).
ferent temperatures. Below we discuss patterns in ant thermal tol- Indeed, the pattern of lower critical thermal limits in nocturnal ants
erance at two scales, seasons and days, then review evidence for compared to higher critical thermal limits in diurnal ants appears
acclimation. widespread and has been documented across the globe (Kay and
Whitford 1978, Cerdá et al. 1997, Jayatilaka et al. 2011, Garcia-
Seasonal Robledo et al. 2018). Temporal differences in thermal tolerance are
not restricted to cross species comparisons though as workers of
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Seasonal changes represent a yearly challenge for ants as temperat-
ures cycle from the cold of winter to the warmth of summer—a phe- Ectatomma ruidum that are active during the day also have higher
nomenon that increases with latitude, particularly in the northern CTmax than those active at night (Esch et al. 2017, Nelson et al. 2018).
hemisphere (Sheldon and Tewksbury 2014). Few studies have exam- One relationship of continued interest for ant biologists looking
ined if thermal tolerance parallels seasonal patterns in temperature, at daily patterns of temperature and activity is the dominance-
yet those that have present compelling evidence. For example, com- thermal tolerance tradeoff. This hypothesis posits that behavior-
munity means of heat tolerance for five ant species in Oklahoma ally dominant species control resources at thermally optimal times
were on average 3.8°C higher in summer than in winter (Fig. 2) and of the day, while subordinate species with potentially higher or
ants that were active across spring, summer and winter also showed lower thermal tolerances are forced into less optimal foraging times
greater plasticity in heat tolerance than bi-seasonally active species characterized by thermal extremes (reviewed in Cerdá et al. 2013).
(Bujan et al. 2020b). Likewise, intraspecific patterns of thermal tol- Examples supporting the dominance-thermal tolerance tradeoff are
erance tracking seasonal variation in temperature have been docu- abundant and exist in communities from disparate habitats like de-
mented in the ant genera Myrmecocystus, Myrmica, and Wasmannia serts, forests, grasslands, shrublands, and urban lawns (Cerdá et al.
as workers have higher CTmin and/or CTmax in warm compared to 1997, Cros et al. 1997, Cerdá et al. 1998, Bestlemeyer 2000, Lessard
cool months (Kay and Whitford 1978, Maysov and Kipyatkov et al. 2009, Wiescher et al. 2011, Roeder et al. 2018). There are
2009, Coulin et al. 2019). Seasonal patterns of thermal tolerance caveats as behavioral dominance likely varies across communities
are not always consistent though as plasticity among congeners can and habitats with different environmental conditions. Teasing out
vary within a single location (Kay and Whitford 1978, Bujan et al. the causal variables in these relationships will require studies that
2020b). Why some, but not all, species demonstrate seasonal plas- measure thermal tolerance in combination with foraging behavior
ticity in their thermal tolerance remains puzzling and should be a and environmental temperatures—a holistic approach that is not al-
topic of future interest for ant thermal biologists. ways done.
Acclimation
Thermal acclimation is generally a reversible physiological change
that enhances performance in response to environmental condi-
tions (Angilletta 2009). Different from thermal adaptation, which
focuses on the evolution of phenotypes, acclimation occurs on a
shorter time scale and has primarily been measured in laboratory
studies (Jumbam et al. 2008, Chown et al. 2009, Oms et al. 2017,
Bujan et al. 2021). Interestingly, findings from Cahan and col-
leagues (2017) suggest Aphaenogaster ants acclimated to higher lab
temperatures have higher baseline expression of three heat shock
protein genes: Hsc70-4, Hsp40, and Hsp83. Thus, acclimation to
varying temperatures involves heat shock responses and may be
one reason why such ants exhibit higher thermal tolerances, an
induced thermotolerance so to speak (Evgen’ev et al. 2007). Ants
developing under warmer thermal conditions may likewise exhibit
higher thermal tolerances as seen in Aphaenogaster senilis (Oms
et al. 2017) and hypothesized in Aphaenogaster iberica (Villalta
et al. 2020). Cuticular hydrocarbon composition has also been
linked to thermal tolerance in ant colonies acclimated to different
temperature treatments and may play a role in resisting desicca-
tion (Menzel et al. 2018). It remains unclear how long it takes for
Fig. 2. Plasticity in heat tolerance (i.e., CTmax) for five ant species across
three seasons. Redrawn with permission from Bujan et al. 2020b. Ant
thermal acclimation to occur as no evidence of acclimation was ob-
images were taken by April Noble and Jen Fogarty from www.AntWeb.org served for Ectatomma ruidium after 3 h (Nelson et al. 2018), while
(Specimen codes: CASENT0005320, CASENT0005669, CASENT0005321, Myrmecocystus depilis was able to acclimate after 25 h but only at
CASENT0005804, CASENT0102869). temperatures above 35°C (Kay and Whitford 1978).464 Annals of the Entomological Society of America, 2021, Vol. 114, No. 4
Other Sources of Variation for Ant Thermal Body Size
Tolerance Is body size an important correlate of thermal tolerance? One
thought is that larger ants should be able to tolerate both colder and
Potential variation in ant thermal tolerance exists beyond the pre-
hotter temperatures either because their morphology (e.g., longer
viously described patterns along spatial and temporal gradients. We
legs) enables them to escape detrimental microclimates (Cerdá and
focus on sources that have been either regularly acknowledged (evo-
Retana 2000) or through better mitigation of harmful physiological
lutionary history and body size) or rarely mentioned (age, castes and
processes (Chown and Nicolson 2004). Yet, observed relationships
nutrition).
between thermal tolerance and body size are complex and rarely
consistent. In polymorphic ants like Atta sexdens, Cataglyphis
Evolutionary History velox, and Eciton burchellii, a positive relationship exists between
Ants are an incredibly diverse clade with a fossil record dating back higher heat tolerance and a larger body size (Cerdá and Retana
ca. 100 million years and molecular data suggesting divergence from 1997, Ribeiro et al. 2012, Baudier and O’Donnell 2018), but
evolutionary close relatives sometime around the late Jurassic to this pattern has been inconsistent for Solenopsis invicta (Bentley
early Cretaceous (Brady et al. 2006, Moreau et al. 2006). We obvi- et al. 2016, Wendt and Verble-Pearson 2016, Lytle et al. 2020).
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ously do not have thermal trait data from these time periods, how- For monomorphic ants like Aphaenogaster senilis, Temnothorax
ever understanding evolutionary history may provide insight into curvispinosus, and Ectatomma ruidum, there has been little to no
patterns of thermal tolerance along the ant phylogeny that we can evidence of a positive size-tolerance relationship (Esch et al. 2017,
observe today. In Drosophila flies, for example, upper thermal limits Oms et al. 2017, Yilmaz et al. 2019, but see O’Donnell et al. 2020)
are phylogenetically constrained as related species exhibit com- suggesting intraspecific variation in upper thermal limits may be
parable levels of heat resistance (Kellermann et al. 2012). Similar constrained to species with a polymorphic worker caste. The link
phylogenetic signals in heat tolerance have been recorded for ants between lower thermal limits and body size, while rarely investi-
using large datasets (Fig. 3; Diamond and Chick 2018b, Bujan et al. gated within a species, has yielded similar mixed results with either
2020a), but this result has not been consistent (Arnan and Blüthgen no pattern (Yilmaz et al. 2019) or positive (Hahn et al. 2008), nega-
2015, Bishop et al. 2017, Nowrouzi et al. 2018). Moreover, there has tive (Bentley et al. 2016), and hump-shaped relationships (Baudier
been a general lack of phylogenetic signal in cold tolerance of ants and O’Donnell 2018). Across species, tolerance-size relationships
(Bishop et al. 2017, Bujan et al. 2020a, but see Diamond and Chick have been uncovered in tropical ant assemblages (Kaspari et al.
2018b). One issue that all current ant studies must contend with is 2015) as well as within specific clades like army ants (Baudier et al.
the lack of a resolved species level phylogeny. Instead, researchers 2018). But again, these results vary as CTmax declined with body
commonly rely on genus level trees, limiting detection of phylogen- mass in temperate and montane assemblages (Verble-Pearson et al.
etic patterns. 2015, Nowrouzi et al. 2018).
Age and Castes
Ant colonies typically consist of one or more queens, workers,
brood (i.e., eggs, larvae, and pupae), and sometimes reproductive
alates. Workers experience the greatest variance in temperature
given their role in nursing young, maintaining the nest, foraging
for resources, and providing defense (Hölldobler and Wilson
2009). Alates fly during warm periods of the year and must en-
dure hot temperatures that sometimes reach over 50°C (Dunn
et al. 2007, Helms 2018). Queens and their brood, however, are
buffered from extreme temperatures by soil, leaf litter, and vege-
tation surrounding the nest (Jones and Oldroyd 2006, Kadochová
and Frouz 2013). One might posit that ants of different age and
caste would consequently exhibit different tolerance values given
the variance in thermal environment they experience, as seen in
tropical butterfly species (Klockmann et al. 2017). Yet current evi-
dence is mixed for ants. For example, no difference was found be-
tween CTmin, CTmax, and the ability to acclimate for Wasmannia
auropunctata queens and workers (Coulin et al. 2019). In contrast,
newly eclosed adults (i.e., callows) of the subterranean army ant
Laibus praedator are less cold tolerant before their cuticle hardens
(Baudier and O’Donnell 2016). Moreover, the supercooling points
of hibernating Leptothorax species are similar in adult workers
and larvae (Heinze et al. 1996), but nurse workers compared to
foragers of Temnothorax acorn ants have increased survival rates
under high temperature/low humidity conditions (Menzel et al.
2018). The age of an individual may thus be an important deter-
minant of its thermal tolerance (Bowler and Terblanche 2008),
Fig. 3. Cold and heat tolerance (i.e., CTmin and CTmax) of 39 genera across the but this has rarely been tested because measuring thermal traits
ant phylogeny. Redrawn with permission from Bujan et al. 2020a. throughout development remains challenging.Annals of the Entomological Society of America, 2021, Vol. 114, No. 4 465
Nutrition a handful of species. Are results consistent across the ant phy-
While thermal tolerance may or may not have strong relation- logeny? Moreover, how important are genetic differences within
ships with individual characteristics such as age and size, nutri- and across populations of the same species?
tion plays an important role. Worker nutrition has been linked to 6. Castes—Almost no studies have examined differences in thermal
higher thermal tolerance as colonies with access to greater carbo- tolerance between reproductive alates and workers. Species
hydrate resources may be able to tolerate higher temperatures distributions are commonly modeled using worker tolerance
(Bujan and Kaspari 2017). Similar results have been observed in values, but those predictions might be an underestimate or
fruit flies (Nyamukondiwa and Terblanche 2009), although results overestimate of true geographic distribution if winged alates
are sometimes inconsistent or more complex than originally thought are able to tolerate different thermal conditions. Such tolerance
(Andersen et al. 2010, Mitchell et al. 2017). One mechanism for differences are especially important for projecting future range
this phenomenon is that ingested sucrose can be stored as the disac- sizes of invasive species.
charide trehalose or glycogen (Sacktor 1970, Schilman and Roces 7. Climate Change—The world is changing. Yet we know little
2008) and then used to quickly generate adenosine triphosphate or about how or even if physiological traits of ants are following
ATP (Suarez et al. 1996). ATP enables the synthesis of heat shock suit. Moreover, are ants from the tropical regions indeed more
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proteins and is highly correlated with an organism’s ability to tol- threatened by climate change than their temperate counterparts?
erate higher temperatures (King and MacRae 2015). Collecting data now will be imperative for answering questions
in future decades about thermal adaptation.
Conclusions and Future Directions
Supplementary Data
Occupying numerous ecosystems and their variable climates, ants
Supplementary data are available at Annals of the Entomological Society of
and their thermal tolerances have captured the attention of re- America online.
searchers worldwide. From understanding daily patterns in activity
to testing hypotheses across geographic gradients, the field of ant
thermal tolerance continues to grow. Yet much remains to be dis- Acknowledgments
covered. Throughout this review, we have discussed methods, pat- We thank all of the ant and thermal biologists who have made this review pos-
terns, hypotheses, and potential sources of variation in ant thermal sible, especially Marshall McMunn who was instrumental in the initial brain-
tolerance. There exist numerous topics to explore further and we storming phase. Early drafts were improved by feedback from Jesse Daniels
highlight seven, each representing an area in need of additional and Anna Paraskevopoulos. Mention of trade names or commercial products
research. in this publication is solely for the purpose of providing specific information
and does not imply recommendation or endorsement by the U.S. Department
1. Methods—Comparative studies looking at different methods are of Agriculture. USDA is an equal opportunity provider and employer.
lacking. The few that exist primarily focus on ramping rates in
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