Thermoregulation strategies in ants in comparison to other social insects, with a focus on red wood ants ( Formica rufa group)

Version Changes

Revised. Amendments from Version 1

In this second version of our review paper we have incorporated comments and changes suggested by referees. Those changes include a change of title suggested by Dr. Sovary, which now better captures the range of ants described in the paper. Other changes include broadening of the introduction to include the main idea that two thermoregulatory strategies can be found in mound building ants, more detailed description of nest moisture changes during natural forest succession (gradual increase of shading and change from dry thermoregulation strategy in young nests to wet nest strategy in big mature colonies), and the addition of information regarding exchange of respiratory gases in the paragraph about Atta nest ventilation systems. We also shortened and rewrote some of the paragraphs about thermoregulation in Formica rufa group as suggested by the referees to make the main message of the review more clear. There have been minor changes (namely formatting) in the reference list and one reference was replaced. In Table 1 a thermoregulatory strategy column was added to divide the species into “brood movers” and “stable temperature nest”. Also the description of the thermoregulatory characteristics in the Formica rufa group was improved. The authors thank the referees for their review and comments to our paper. Most of suggested changes have been included in the latest version of the paper. For more details and explanation of the changes included and omitted please see the referees’ comments and authors’ replies.

Abstract

Temperature influences every aspect of ant biology, especially metabolic rate, growth and development. Maintenance of high inner nest temperature increases the rate of sexual brood development and thereby increases the colony fitness. Insect societies can achieve better thermoregulation than solitary insects due to the former’s ability to build large and elaborated nests and display complex behaviour. In ants and termites the upper part of the nest, the mound, often works as a solar collector and can also have an efficient ventilation system. Two thermoregulatory strategies could be applied. Firstly the ants use an increased thermal gradient available in the mound for brood relocation. Nurse workers move the brood according to the thermal gradients to ensure the ideal conditions for development. A precise perception of temperature and evolution of temperature preferences are needed to make the correct choices. A second thermoregulatory strategy used by mound nesting ants is keeping a high temperature inside large nests. The unique thermal and insulation properties of the nest material help to maintain stable conditions, which is the case of the Wood ant genus Formica. Ants can regulate thermal loss by moving nest aggregation and alternating nest ventilation. Metabolic heat produced by ant workers or associated micro organisms is an important additional source of heat which helps to maintain thermal homeostasis in the nest.

Introduction

Temperature is an important factor for all ectothermic organisms, including ants. Their rate of development is accelerated with high temperatures ¹, the movement rate speeds up ² and the rate of food and oxygen consumption also increases ³. Higher temperatures can be advantageous for colony fitness as it can increase reproduction rate though at the same time can be disadvantageous due to higher energy expenditure ⁴.

Most insect species have a solitary mode of life in adulthood; these individuals are able to regulate their body temperature through behavioural reactions such as sunning or seeking cool shelter ⁵. More sophisticated forms of thermoregulation can be found among social insects. They are able not only of regulating their own body temperature but also the temperature of the immediate surroundings. This ability is due to the large number of individuals in the society, their behavioural interactions and nest construction ⁶. The nest protects the whole colony and serves as a shelter for adults and, more importantly, as an incubator for the brood. Improved colony homeostasis could even be one of the reasons why insect sociality evolved ⁵. Thermoregulation, however, requires the expenditure of energy and so comes with costs as well as benefits.

The level of nest thermoregulation depends on many other factors, e.g. nest size, population size, and the moisture and thermal conductivity of the nest material. Among mound building ants two main thermoregulatory strategies can be distinguished: 1) moving the brood according to thermal gradients (natural or induced) and 2) keeping stable temperatures inside their nests. This paper’s objective is to provide an overview of nest thermoregulation strategies occurring among ant societies, with a focus on thermoregulation in the red wood ants ( Formica rufa group), in comparison to other social insects.

Nest architecture and properties of nest material

Ants nest in wide range of materials; in soil, under stones, in leaf litter and even in living trees (see Table 1). Some of them build above-ground nests, usually from soil or organic material, called ant hills or mounds. These nests show an advanced ability in regulating inner temperature.

Table 1. Examples of thermoregulation and nesting strategies in social insects.

Thermoregulation characteristic	Thermoregulation strategy	Nest type	Taxa and species involved	References
Temperature is stable, same as the temperature of the soil	Brood translocation	Underground nests only	Ants: Tetramorium tsushimae, genus Lasius and Myrmica, Pogonomyrmex; Termites: genus Coptotermes	Hólldobler & Wilson (1990) 23, 47, Sanada - Morimura & al. (2005) 59
Temperature is not stable, nest follows microhabitat temperature - oscillations can be buffered by insulation properties of microhabitat, sometimes natural structures can be used as heat accumulators	Brood translocation	Nests in wood (logs or stumps), in leaf litter, and under stones	Ants: Acromyrmex ambiguus, Camponotus mus, C. vicinus, Myrmica punctiventris Roger, Onychomyrmex hedleyi, Polyrhachis simplex Termites: Kalotermitidae, Hodotermitidae, Rhinotermitidae, Termopsidae	Banschbach & al. (1997) 32, Bollazzi & Roces (2007) 30, Roces & Nunez (1989) 29, Chen & al. (2002) 56, Hólldobler & Wilson (1990) 23, 47, Miyata & al. (2003) 58, Ofer (1970) 57
Temperature oscillates, the thermal gradient could be greater than the ambient temperature because the mound surface serves as a solar collector	Brood translocation	Underground nest with aboveground crater or similar structure + above ground soil (soil and fecal pellets mixture) or thatch mound	Ants: Acromyrmex heyeri, genus Lasius, Myrmica rubra, Pogonomyrmex occidentalis, Solenopsis invicta, Termites: Cephalotermes rectangularis, Microceretermes edantatus, Thoracotermes macrothorax	Weir (1973) 39, Bollazzi & Roces (2002) 38, Cassil & al. (2002) 69, Cole (1994) 60, Hólldobler & Wilson (1990) 23, 47, Lüscher (1961) 62, Nielsen (1972) 67
Energy is accumulated by spatial structure - silk caps of pupal cells storing sun energy	Stable temperature	Paper nest	Hornet: Vespa orientalis	Ishay & Barenholz-Paniry (1995) 64
Energy is accumulated by sun bathing ants and is transported into the nest	Stable temperature	Underground nest + above ground organic mounds	Wood ants : Formica rufa, F.polyctena	Coenen-Stass (1985) 14, Frouz (2000) 15, Zahn (1958) 51
Nest is heated by the sun (temperature of peripheral layers oscillates) + inner core with more stable temperature, heated by metabolism of termites or ants	Stable temperature (?)	Aboveground nest in wood (living trees)	Termites: Coptotermes acinaciformis, C. frenchi	Greaves (1964) 65
	Stable temperature (?)	Underground nest + aboveground soil mound	Termites: family Termitidae, Macrotermes bellicosus, Amitermes merionalis; Ants genus Atta - Atta texana, A. vollenweideri	Kleineidam & al. (2001) 27, Hólldobler & Wilson (1990) 23, 47, Korb & Linsenmair (1998, 2000) 25, 42, Grigg (1973) 26
Nest is heated by sun (temperature of peripheral layers oscillates in small nests or stable in big ones) + inner core with stable temperature, heated by metabolism of ants + decay of organic material	Stable temperature	Underground nest + above ground organic mounds	Wood ants: genus Formica – Formica aquilonia, F. rufa, F. polyctena	Coenen-Stass (1985) 14, Frouz (2000) 15, Rosengren & al. (1987) 46, Zahn (1958) 51
Stable temperature inside the cluster is maintained by ant metabolism	Stable temperature	No stable nest - bivouacs	“Army ants” Eciton burcheli, E. hamatum	Franks (1989) 48, Schneirla (1971) 41
Active heating by members using contractions of muscles	Stable temperature	Wax or paper nest in air or various cavities	Honey bees, Stingless bees, Bumble bees, Wasps: Apis mellifera, A. florea, A. dorsata, Bombus sp., Trigona denoiti, Vespa simillima, V.xanthoptera, V. crabro	Fletcher & Crewe (1981) 61, Heinrich (1981) 20, Ishay (1973) 63, Martin (1988) 50, Morse & Laigo (1969) 66, O´Donnell & Foster (2001) 68

The red imported fire ant Solenopsis invicta and members of the genus Pogonomyrmex build soil mounds from excavated soil ^{7, 8}. These nests gain heat through solar radiation and the brood is moved along an increased thermal gradient ^{1, 9}. Weaver ants from the genus Oecophylla construct their nest from living leaves, with the help of their own larvae, which produce a special “glue” from their salivary glands ¹⁰.

Red wood ants from the genus Formica build large nests from organic material that is based on a mixture of soil, twigs, coniferous needles and pebbles ^{3, 11– 13}. In these nests a stable heat core can be maintained thanks to the good insulation properties of these materials and the metabolic heat produced by the ants or their associated microflora ^{14, 15}.

The composition of the organic material is not the same throughout the whole nest volume ^{3, 16} and the mound structure is not rigid either. The ants loosen and renovate the nest structure and the organic material is continuously moved from the inside to the outer layers ³. Nest structure and architecture plays a vital role in nest thermoregulation. The tunnels and passages build by ants are important mainly for ventilation and humidity control, which affect the nest temperature. Pieces of tree resin are often incorporated into the Formica nest material because of its antimicrobial effect ¹⁷. The resin inhibits the growth of potentially pathogenic bacteria and fungi in the nest.

Thatch ants, Formica obscuripes ¹⁸ and Acromyrmex heyeri ¹⁹, use plant fragments as a building material and arrange them in a thick compact surface layer called “thatch” which has a lower thermal diffusivity than the surrounding soil. The thatch prevents nest overheating by the incoming solar radiation and avoids losses of the accumulated heat into the cold air during night ¹⁹.

Nest moisture can have two different and opposite thermoregulatory effects: 1) moisture can support microbial heat production (i.e. increase the temperature) ^{3, 15}; 2) it can decrease the insulating properties of nest material (i.e. decrease the temperature) ¹¹. A study of the relationship between daily temperature regime and moisture in Formica polyctena nests revealed two possible thermoregulation strategies which differ between dry nests and wet nests ¹⁵. Dry young nests are usually located in sunny open places ¹². Solar radiation heats up the nest and keeps the nest material dry, with low heat capacity and conductivity. The thermal losses of dry nests are estimated to be 0.15–4.3 W per nest ¹⁵. The temperatures of dry nests are usually the highest in the evening and they drop during the night. Thermoregulation in dry nests is based on a combination of metabolic heating from the ants, the insulating properties of the nest and solar heating ¹⁵.

During forest succession, ant nests become more shaded and gradually switch to a wet thermoregulation regime ¹². In the evening the temperature in these nests is low and it increases during the night. The high night temperature at the nest surface indicates substantial heat loss, about 24–30 W per nest. The wet nests have a high thermal capacity; increasing the temperature by 1°C requires a thermal input of 35 W ¹⁵. This means that maintaining a sufficient temperature in a wet nest requires a heat source beyond the metabolic heat produced by ants and the heat obtained from solar radiation. The additional heat source in wet nests is provided by microbial activity ^{3, 15}. Both of these two types of thermoregulation strategies are applied in natural populations, but in different stages of nest development. The microbial community in F. polyctena nests differs from that in the surrounding soil in part because of differences in pH and food availability and quality ¹³. Thermoregulation via microbial heating was first proposed in 1915 by Wasmann ³. In 1980 the existence of microbial heating in F. polyctena mounds was confirmed in an experiment showing that in the absence of ants non-sterilized nest material generated a substantial amount of heat but sterilized nest material generated almost no heat ³.

Microbial activity can be estimated by calculating the respiration rate of the nest material, which is used as a proxy for the respiration rate of the microbes living in it ^{3, 15}. There are detectable seasonal changes in the respiration rates of nest material with the highest rates found in summer. The mass-specific heat production of ants is higher than that of the nest material but, when considering the total mound volume, microbial heat production is more than seven times higher than the heat evolved by ants ³. Ants can affect microbial activity via nest material aeration, supply of fresh plant material and their own metabolic heat production. Since the microbial activity of wet nest material depends strongly on temperature ³, a temperature increase in some small parts of the nest (due to ant metabolism or sun radiation) results in an increase in microbial activity and consequently in a subsequent overall increase of nest temperature.

As first mentioned by Forel in the early 1920s the ant mound often serves as a solar collector ²⁰. Solar energy can both increase the metabolism of ants and help heat the nest mound ²¹. Compared to underground nests, mounds absorb heat more quickly both in the direct sun and in the shade ⁹. Ants in the Northern Hemisphere usually remove shading grass from the south side of the mound so that the temperature increases quickly on that side. This creates a temperature gradient that many species use for brood displacement ⁹. Other species decorate the mound surface with small pebbles or dead vegetation, which can work as heat collectors or as radiation reflectors ²².

Mounds of some Formica, Solenopsis and Lasius species are asymmetric, with the main axis oriented in a south-north direction ^{23, 24}. In S. invicta the angle of the south slope of the mound is negatively correlated with the maximal sun angle ²². Sun-influenced thermoregulation in termites has also been documented, for example in fungus-growing members of the genus Macrotermes ²⁵. The amount of intercepted sunlight influences the shape of termite mounds and leads to great structural differences in nests in forests vs. savannahs ²⁵. But the most admirable sun-induced nest shape differences can be seen in Australian “magnetic termites” Amitermes meridionalis ²⁶. The nests are wedge-shaped with apparent north-south orientation which prevents overheating at noon and enables maintaining the warmth of nest in the evening.

Effective ventilation takes place as part of nest thermoregulation in many ant species, being regulated by the opening and closing of nest entrances (see below). A ventilation system in nests of the leaf-cutting ant genus Atta was described by Kleineidam et al. ²⁷. There is not a thermal gradient big enough to generate thermal convection flow; rather the ventilation in Attini nests is driven by the wind. There are many openings on the nest surface, which are functionally divided into entry and exit tunnels. Wind flowing over the nest from any direction causes air to exit from the central tunnel and to enter tunnels at the nest periphery ²⁷. This ensures exchange of respiratory gasses and optimal thermal conditions for symbiotic fungi which are damaged by temperatures higher than 30°C ²⁸.

Behavioural reactions of ant workers

Behavioural reactions of ants are based on sensing temperature and temperature preferences ⁵. To react to these gradients, ants have evolved inherent temperature preferences, which are the key element in thermoregulatory behaviour ^{4, 29}. Nurse workers are able to choose the optimal temperature for pupae production and sexual brood incubation and to move the brood along temperature and humidity gradients to achieve the best conditions for its development ^{5, 29, 30}.

The optimal temperature range is variable for different groups of social insects, for example the brood of the honey bee Apis mellifera develops fastest at 35°C ³¹. In Formica polyctena a temperature 29°C is preferred for pupal development ¹⁴, whilst colonies of Solenopsis invicta can grow only between 24 and 36°C ¹. In contrast the genus Myrmica is adapted to cold climates, M. rubra ⁴ and M. punctiventris ³² prefer temperatures between 19 and 21°C, about 8°C lower than the temperature preferred by other ants.

Temperature preferences can be affected by many factors including age and sex ³³, working caste or feeding condition ¹, or prior acclimation ³⁴. Ant queens in Formica polyctena ³⁵ and Solenopsis invicta ¹ prefer slightly higher temperatures than workers, especially during the egg-laying phase; inactive queens may prefer cooler temperatures. Workers generally prefer lower temperatures, which decrease their metabolic rate and increase their lifespan ^{1, 36}. A decrease of 2°C can lengthen the worker lifespan in S. invicta by 14% ³⁷. Preferences of nurse workers tend to be shifted towards the higher temperatures that favour brood development ^{1, 4, 21, 29}. Similar patterns have also been found in Apis mellifera ^{5, 31}.

Most ant species rely on brood translocation along temperature gradients as the main thermoregulatory strategy ^{6, 9, 23, 29, 30, 38}. The brood translocation usually has characteristic time rhythms, for example Camponotus mus follow a photoperiodic circadian rhythm. In the presence of a temperature gradient, nurse workers move the brood twice each day ²⁹. The first displacement starts at 2 pm, when the brood is transported from the colder night location to a warmer day location. This movement occurs 6 h after sunrise, i.e., in the middle of photophase. At 10 pm (8 h after the first displacement and 2 h after nightfall), the brood is transported back to the night location. Under artificial light/dark day cycles the brood translocation rhythm changes according to the new photophase length ²⁹. In Solenopsis invicta moving the brood up and down along temperature gradients does not seem to depend on the time of day or photoperiod ⁹.

In response to temperature gradients, leaf-cutting ants from the genus Acromyrmex move not only the brood but also the symbiotic fungi which provide their food. The fungus requires high humidity and temperatures between 25 and 30°C ²⁸. Acromyrmex ambiguus workers move the fungus garden according to humidity conditions, but they are also capable of nest humidity regulation by changing nest architecture. The flow of dry air into the colony is a signal for workers to plug ventilation tunnels to prevent nest from drying out ³⁸. Similar behaviour has been proposed for termites ³⁹.

When the nest interior becomes too hot, workers can reduce the inner temperature in several ways. In ants and termites nest cooling is usually achieved by changes in building behaviour. Workers of leaf-cutting ants in the genera Atta and Acromyrmex open tunnels to allow air circulation ^{27, 30, 38}; this behaviour could be limited by a trade off for humidity control ⁴⁰. Ants of the genus Formica can also partly remove the nest material, which reduces the wall thickness and increases heat dissipation ¹⁶. In the genus Eciton, loosening of bivouacs´ structure (temporary nests similar to a honeybee swarm) is an effective way of cooling ⁴¹.

Even more efficient ventilation systems providing both temperature regulation and respiratory gas exchange can be found in nests of the termite Mactorermes bellicose. These nests can have either externally or internally driven ventilation, depending on the habitat, nest shape (cathedral vs. dome shaped nest) or the time of day ⁴². Cathedral shaped nests in open habitats are warmed by the sun, which creates a steep thermal gradient leading to convention currents in peripheral air tunnels. Dome shaped nests located in the forest rely more on internally driven ventilation. The same is true for cathedral nests at night ⁴².

In contrast, bees, wasps and bumblebees cool their nests by wing-fanning and regurgitating water droplets. Water is spread over the brood comb surface enabling cooling through evaporation ⁵. Cooling by water evaporation is very effective. Lindauer ⁴³ placed a bee hive onto a lava plain where the surface temperature reached 70°C. Taking water ad libitum, the bees were able to maintain the hive temperature at the favoured 35°C.

Some social insect species have evolved highly elaborated systems of thermoregulation that enable to keep stable temperatures inside their nests. Bees, bumblebees and wasps are capable of direct incubation of selected pupae. Specialized workers sit on the surface of the brood cell and maintain their thoracic temperature over 35°C. Bees sitting inside empty brood cells can heat six brood cells at one time ⁴⁴. Metabolic heat can also be used for protection, as shown in the interaction between the predatory hornet Vespa mandarina japonica and Japanese honeybees Apis cerana japonica ⁴⁵. If the hornet attacks a honeybee nest it is surrounded by bee workers who increase their body temperature to a level which is lethal for the hornet but not for the honeybees ⁴⁵.

Although ants cannot actively produce heat they are able to use indirect metabolic heat (i.e. heat produced as a by-product of metabolism) for ensuring brood development. This ability has so far been postulated for the Formica rufa group ^{3, 15, 46} and the army ant genus Eciton ^{41, 47, 48}.

The Neotropical army ants Eciton hamatum and Eciton burchelli form temporary swarms called bivouacs, which can regulate temperature very precisely to ensure optimal conditions for developing brood ⁴¹. According to Franks ⁴⁸ bivouacs have a similar construction to a bee swarm; they can be divided into an outer mantel and inner core, which together maintain a stable temperature between 27.5 and 29.5°C regardless of the ambient temperature. On cold days the bivouacs change shape: they become more hemispherical to reduce the surface to volume ratio ⁴⁸. Franks ⁴⁸ postulates that all the heat required by the bivouac can be produced by ant metabolism.

Red wood ants of the Palearctic genus Formica ( Formica rufa group) are supposed to use metabolic heat to maintain a heat core, an area with high and stable temperatures, in their nests. High temperatures are required for sexual brood development; nests producing sexual offspring always have higher temperatures than those producing only workers ⁴⁶. The heat core’s position moves according to nest shape and size ^{3, 15}. The temperature inside nests of red wood ants begins to increase very early in the spring, even when the nest surface is covered by ice and snow ⁴⁶. At this time some nests can contain larvae, pupae, and even some winged individuals, indicating that the inner heating must have started much earlier, because larval development cannot start in a cold nest and requires some weeks of constant warm temperature ²¹. It is supposed that in large nests of F. rufa containing over 1 million workers, spring nest heating can start as an autocatalytic process ⁴⁶ that relies on utilizing lipid reserves in young workers ⁵⁰.

Another factor contributing to quick spring increase of nest temperature in red wood ants is a temperature intake by ant bodies. The Formica ants are dark colored so they heat up quickly when exposed to the sun during their outside-nest activities. In the spring ants are observed to create clusters on the mound surface as they bask in the sun ⁵¹. Their bodies contain a substantial amount of water which has high thermal capacity making ant bodies an ideal medium for heat transfer. After getting hot enough the ants move inside the nest where the accumulated heat is released. This principle works throughout the year but in spring it is most obvious and supported by ant clustering on the nest surface ^{15, 46}.

Daily temperature fluctuations in the red wood ants nest seem to be correlated with temperature-dependent changes in ant density and ant aggregations in the nest. The highest nest temperatures usually occur in the afternoon or in the evening which corresponds with the return of foragers ^{15, 46}. This apparently results from the heat brought into the nest by returning workers (heat coming from absorbed solar energy) as well as the heat generated by worker metabolic heat production within the nest. In some nests the temperature drops slightly in the morning when ants leave the nest ^{15, 16}. Heat coming from the metabolism of foragers clustered in the nest center on cool days, when ambient temperature limits outdoor activities, could also explain a negative correlation between the inner nest temperature and the ambient temperature found occasionally in spring ⁴⁶.

The seasonal fluctuations in the thermoregulation behaviour of Formica polyctena along a geographic gradient were studied by Frouz & Finer ⁴⁹. Both in Finland and the Czech Republic the ant colonies maintained a high nest temperature (over 20°C) in spring and summer, for about 65–129 days. A rapid increase in the inner nest temperature in early spring was observed, mostly at the beginning of April. Annual nest temperature peaked in June in both locations and decreased gradually from August to November. Nest temperatures fluctuated more in the Czech Republic than in Finland, possibly because of greater differences between day and night ambient temperatures ⁴⁹.

An interesting question is why F. polyctena maintain stable nest temperatures for the same period in Finland and the Czech Republic even though the length of the vegetation season and the ambient temperatures in Finland and Czech Republic are different. This might be explained by the reproduction cycle of the queen. Regular shifts between reproduction and diapauses has been documented in F. polyctena queens. The queen enters diapauses after 100 days of reproduction even at a constant temperature and photoperiod ^{35, 52}. It was postulated that ants maintain high temperatures only during the queen’s reproduction phase ⁴⁹. After that the nest temperature drops, despite the fact that the outside temperature usually does not limit foraging and the ants are still active.

Use of metabolic heat for nest thermoregulation in ants

Maintenance of a high inner nest temperature has been observed in ants, especially in species which build above-ground nests or inhabit tree hollows ^{15, 46, 53}. Heating of these structures is much easier than heating underground nests, because the surrounding soil has a large heat capacity and conductivity.

In moderate climates most ants build nests in the soil where the temperature is quite stable ( Table 1) or on the soil surface under a layer of leaf litter where the temperature can be buffered by the insulating properties of the nest material. Many species in the Northern Hemisphere also nest under rocks or stones which serve as heat collectors ( Table 1). In the tropics only a few species nest in soil and the majority of species inhabit small pieces of rotting wood ⁵. More precise microclimate regulation is achieved in the mound-building species of the genera Atta, Acromyrmex, Myrmicaria, Pogonomyrmex, Solenopsis, Iridomyrmex, Formica, and Lasius ( Table 1).

The maintenance of a stable temperature in red wood ant genus Formica nests during spring and summer is widely known and has been the subject of many studies ^{12, 16, 46, 49, 53}. These ants are able to maintain thermal homeostasis in the nest because of the insulation and heat storage provided by the nest material ^{15, 20}. Mound size is generally correlated with the number of inhabitants ^{54, 55}. In small nests located in sunny areas the solar radiation and the insulation properties of the nest material are thought to be the key elements in nest thermoregulation ^{11, 12}. In larger nests there are internal sources of heat production, such as ant and microbial metabolic heat, that enable the maintenance of high inner temperatures even in a permanently cold environment ^{46, 49}.

Many other ant species (see Table 1) build hill-shaped nests from soil. These nests show large spatiotemporal variations in temperature and ants select the optimal temperature for brood development by brood displacement ¹. These nests, however, do not have a stable heat core. The heat core where the temperature is stable and higher than ambient temperature for an extended period of time (several months) can be found only in a minority of ant species. Why is this the case?

The heat core exists in the nests/hives of winged insects that are capable of active heating, i.e. bees, wasps, bumblebees (thermogenesis in flying muscles), and some ants, especially the genus Formica ^{3, 15, 46}, the army ant genus Eciton ^{41, 47, 48} and probably in fungus-growing termites ⁴². But there is no evidence of a stable heat core in Solenopsis invicta or in Acromyrmex heyeri, which also build upper-ground hills from materials with suitable insulation properties such as soil or dead vegetation. As discussed earlier, thermoregulation can also be the result of nest architecture, and only those species that build nests with a low thermal heat capacity and a low thermal conductivity are likely to maintain a heat core. In summary, the use of metabolic heat production for maintenance of a heat core depends on the insulation properties of the nest and the size of the individual workers and of the entire colony.

The latest review about nest thermoregulation in social insects ⁶ distinguished three types of ant thermoregulation strategies: “First, like many social bees, some ant species rely on protection from a cavity, such as a tree stump or underground burrows ⁵⁶. Second some migrate their nest frequently, varying the amount of cover they select, depending on the temperature and season ^{57, 58}. Third some others move their brood to areas of optimal temperature within the same nest” ²⁹. We suggest dividing the last category in the following way: a) ants that move the brood in daily cycles to places with optimal temperatures within the whole nest structure, for example Solenopsis invicta ⁹ or Camponotus mus ²⁹ b) ants that keep a stable heat core inside their nest and do not move the brood from the nest interior, including the ants from Formica rufa group ^{3, 15}.

Conclusion

Despite a wide variety of thermoregulatory strategies observed among ant societies some general trends can be found. Two opposite thermoregulatory strategies in mound building ants could be distinguished. Firstly nests with low insulative properties which work as solar collectors and thus increase the available thermal gradient for brood development. Secondly nests which steadily maintain higher inner temperature thanks to low thermal conductivity of the nest material, good insulative properties and metabolic heat produced by ants or associated micro organisms. An example of this strategy is seen in the Formica rufa ant group.

Funding Statement

The author(s) declared that no grants were involved in supporting this work.