Chapter 12 Foraging and Defence Strategies

Anna Dornhaus and Scott Powell

12.1 Introduction 12.2 Acquisition of resources

In many habitats, the first that a visitor is A resource acquisition strategy used by has to likely to notice is an forager. Ant foraging solve several specific problems. Most obviously, a trails can stretch for hundreds of metres, like pseu- relatively small number of foragers have to retrieve dopodia from the central body of the colony, enough food to feed the entire colony. Frequently, searching for and retrieving food. Attempts to less than 10% of workers participate in foraging (the interfere with these foraging trails may prompt a other workers perform brood care and other in-nest rapid and aggressive response from the ants, with tasks, or are inactive, e.g. Dornhaus et al. 2008; Rob- individuals readily sacrificing their life in defence son and Traniello 2002). Contrary to many solitary of the harvested resources. Such conspicuous ac- , ants therefore perform ‘central place forag- tivity is, however, only representative of a small ing’: all food must be brought back to a relatively subset of the striking diversity of foraging and immobile central place, the nest. A large body of defence strategies that have evolved in the ants. theory covers the specific constraints and optimal The goal of this chapter is to discuss the diversity strategies in central place foraging (Orians and of individual and collective strategies used by ants Pearson 1979; Ydenberg and Schmid-Hempel to find, retrieve, and defend resources. More spe- 1994). There is also a discrepancy between the size cifically, we review how ants decide when and of the individual foragers and the size of the colony, where to forage, what individual and collective the ‘superorganism’ that needs to be supplied with strategies are used during foraging, and how food. In other , many physiological and eco- ants communicate about food sources. Any forag- logical characteristics are tightly linked to body size, ing strategy is, however, only as effective as the such as home range or territory (Adams 2001; Jetz et defensive strategies that have evolved to safe- al. 2004), metabolic rate, and lifespan (West et al. guard harvested resources. Consequently, we 1999). In ants, both the body size of individual ants also explore the defensive strategies used in the and the mass of their colonies may be important. An acquisition and retrieval of resources from the ant forager will typically forage much farther from environment, and in retaining them at the nest. its nest than a terrestrial solitary of the While the study of foraging strategies has a rich same size, because ant foragers have to cover a history, much is still to be learnt, and defence foraging range large enough to yield enough food strategies remain a relatively understudied topic. for a much larger organism, the colony. For exam- We therefore identify numerous open questions in ple, a leaf-cutting ant may travel several hundred the study of foraging and defence strategies, and metres to a foraging site (Roces 2002). In relation to further discuss general approaches for advancing body size, this is the equivalent of a human and integrating research in this area in the future. travelling 50–100 km (one way) to collect food.

210 FORAGING AND DEFENCE STRATEGIES IN ANTS 211

It comes as no surprise that foraging is one of the time to forage. Solving all these problems is likely most costly activities performed by an ant colony. to require a mix of innate, -specific beha- Costs arise not only in terms of energy used, but vioural rules, and learning abilities to be used by also in the time spent and the mortality risks faced worker ants. We review each of these aspects of by workers as they leave the nest and travel great foraging in the subsequent paragraphs. distances. Interestingly, the energetic costs of forag- ing, relative to the energy gained by this activity, 12.3.1 Deciding when to forage vary widely among species. In harvester ants, the energetic costs of foraging are negligible compared Before specific foraging strategies come into play, to the energy collected (which is over 1,000 times workers have to decide when to initiate foraging. more than the cost per trip), but in some nectar This can be studied at the individual level (how do foraging ants, the ratio of energy gained to energy individual workers decide when to forage) and at expended for the trip is only 3.9 (Fewell et al. 1996). the level of the colony (how many workers are Some ants may thus need to tightly optimize their allocated to the foraging task). The mechanisms of energetic efficiency, whereas for others, minimizing task allocation at the collective level are relevant in the time- and mortality-costs of foraging may be the study of division of labour, which is not dis- more relevant (Nonacs and Dill 1990). cussed here (but see Beshers and Fewell 2001; Gor- Mortality among ants that leave the nest is much don 1996; Tschinkel 2006 for reviews, and also higher than mortality of workers inside the nest; Chapter 10). The decision to become a forager in- foragers may face dangers such as predation, para- volves trade-offs between exploration and exploita- sitism, adverse weather, and simply losing their tion, and between flexibility and specialization (see way (Ho¨lldobler and Wilson 1990; Nonacs and Biesmeijer and de Vries 2001; Blanchard et al. 2000; Dill 1990). This has led to the hypothesis that Dechaume-Moncharmont et al. 2005; Detrain et al. older workers are allocated to foraging because 1999; Jaffe´ and Deneubourg 1992; Robson and Tra- their loss is less costly to the colony than that of niello 2002; Tripet and Nonacs 2004). Age (Ho¨lldo- younger individuals, which have many work-hours bler and Wilson 1990), genetic background yet to live (Moron et al. 2008; see Section 12.3.1). (Robinson et al. 2005a), ‘corpulence’ (i.e. fat content, Facing these difficulties of large foraging distances, Blanchard et al. 2000), body size (Wilson 1980), or high energy and other costs, and high mortality dominance status (Powell and Tschinkel 1999) may outside the nest, ants have evolved a number of affect the probability that a worker will start forag- strategies to improve their success at finding and ing, as will cues and signals from the colony that retaining resources (see also reviews in Carroll food is available (Table 12.1) or needed (Burd and 1973; Detrain et al. 1999; Gordon et al. 2008; Ho¨lldo- Howard 2005). Classic studies often claim that age bler and Wilson 1990; Roces 2002; Traniello 1989; and body size are the main determinants of task Tschinkel 2006). allocation; however, the fact that foragers are, for example, on average older than in-nest workers 12.3 Individual foraging strategies does not prove that task allocation is based on age per se; experience or disease may also play a role An ant leaving the nest to forage has to first search (Moron et al. 2008; Tripet and Nonacs 2004; Woy- for a suitable food patch. Upon discovery, the for- ciechowski and Kozlowski 1998). ager may then have to overcome the prey item or At the individual level, the decision to leave the dissect it into manageable pieces and decide what nest to forage in many ant species is related to load size to carry. Foragers have to navigate back to environmental conditions, in particular external the nest, either in a straight line or by retracing their temperature (Ho¨lldobler and Wilson 1990; Tra- steps; foragers may also memorize the location of a niello 1989; Tschinkel 2006; Table 12.1). Tempera- food patch to be able to return there or recruit to it. ture may influence the expected foraging success, In addition, before even leaving the nest, forager and thus the likelihood that a foraging trip will ants may have to make decisions about the best recoup its costs in a number of ways. As largely 212 ANT ECOLOGY

Table 12.1 Collective strategies used in food retrieval by ants. See Ho¨ lldobler and Wilson (1990: Table 7–8, p. 280) for a more comprehensive list of genera.

Examplary Recruitment strategy Function genera References

Solitary foraging: Foragers Presumably this strategy is Harpegnathos, Ho¨ lldobler and Wilson (1990); leave the nest used if prey are , Maschwitz and Steghaus-Kovac individually and do not distributed, Cataglyphis (1991); Wehner (1987) appear to interact while unpredictable, and can searching for or be carried back by a retrieving prey. single forager. This strategy is often seen in predatory ants preying on other . Tandem running: a Slow recruitment of , Ho¨ lldobler and Wilson (1990: Table successful forager individual ants to Pachycondyla 7–7, p. 273); Mo¨ glich and recruits and leads a potentially hard-to-find (Plate 12) Ho¨ lldobler (1974) single ant back to the sites, such as new nest food source. sites. Also used in recruitment to food, although possibly less frequently. Group recruitment: a May be an evolutionarily Camponotus Ho¨ lldobler and Wilson (1990: p. 276) successful forager intermediate form of recruits a group of recruitment between several nestmates to the tandem running and resource mass recruitment by pheromone trails; often involves both motor and chemical signals from the recruiting forager. ‘Mass recruitment’ by Useful if a food source is Solenopsis, Beekman et al. (2001); Evison et al. pheromone trail: rich but short-lived, or if Monomorium 2008 Ho¨ lldobler and Wilson successful foragers leave it has to be defended (1990); Tschinkel (2006) a pheromone trail back from competitors. to the nest, which is Depending on the reinforced in a positive volatility of the feedback and quickly pheromone, a certain attracts large numbers minimum number of of nestmates. ants are necessary to maintain the trail. Stable trunk trails: Often used for stable Atta, Forelius, Ho¨ lldobler and Wilson (1990) relatively wide, stable resources such as plants Pogonomyrmex trails lead out from the (where leaves or nest and branch into extrafloral nectaries are smaller trails to cover a harvested); may also be FORAGING AND DEFENCE STRATEGIES IN ANTS 213

foraging area. Trunk used where a foraging trails may also be area is systematically cleared of vegetation. covered by a large colony, or as connections between nests of a polydomous colony. Army ant ‘raids’: these Using this strategy, army Eciton, Dorylus, Couzin and Franks (2003); Franks include large numbers ants have the strength in Neivamyrmex et al. (1991); Ho¨ lldobler and Wilson of ants moving in a numbers to overpower (1990) unified foraging front other social that sweeps a tract of colonies, or, in a few forest. A trail network species, to ‘flush out’ a behind the swarm wider variety of consolidates into a arthropod prey from the single column of traffic leaf litter. for returning prey to the nest and allows foragers to return to the raid. Team transport: two or Used for arthropod prey Eciton Anderson and Franks (2001); Franks more ants cooperate in that is too large or (1987); Ho¨ lldobler and Wilson transporting items from cumbersome to be (1990: Table 10–2, p. 389f) the resource back to the effectively transported nest. by a single forager. ‘Bucket brigades’: foragers This strategy is only likely Atta, Anderson et al. (2002); Ro¨ schard and only transport items a to be used where large Acromyrmex Roces (2003) short distance to a colonies harvest large ‘cache station’, where it numbers of items that is picked up by other are unlikely to be ants that transport it to ‘stolen’ from caches; it the next station. has been observed particularly in fungus- growing ants harvesting leaves.

poikilothermic organisms, ants have an increased weather, or may dry up during the middle of the metabolic rate and thus not only a higher rate of day. Most importantly, temperature-dependent for- energy use, but also higher running speed at higher aging by ants provides some of the best evidence temperatures (Hurlbert et al. 2008; Traniello 1989; for interspecific competition (although this has Tschinkel 2006). However, especially in very hot been debated, see Dunn et al. 2007c and Chapter and dry environments, too high a temperature 5). Species occurring in the same habitat often differ may cause desiccation and death (Cerda´ 1998; Ho¨ll- in the temperatures, and thus time of day, during dobler and Wilson 1990). In addition, temperature which they forage. Competitively dominant ants and weather conditions may change the availability typically forage in the morning, and other ant spe- of food items; for example, prey arthropods may be cies forage at staggered times over the course of the inactive at low or very high temperatures, and plant day (Ho¨lldobler and Wilson 1990; Traniello 1989; nectaries may produce low yields in cold or rainy but see Dunn 2007 and references therein). 214 ANT ECOLOGY

12.3.2 Search behaviour 12.3.3 Orientation mechanisms

Once a forager has decided to leave the nest, it can While searching, ant foragers have to use strategies start searching for a food source. Most modelling to track their location relative to the nest entrance, studies of food-search algorithms assume a corre- in order to be able to return there. The ant Catagly- lated random walk (a random walk in which the phis bicolor in particular has become a standard direction of each step correlates with the previous model system for studies of orientation and naviga- direction of movement, Harkness and Maroudas tion (e.g. Mu¨ ller and Wehner 2007; Wehner and 1985) rather than a systematic search strategy Menzel 1969; Wittlinger et al. 2006). Cataglyphis (such as searching in an expanding spiral; Figure ants use a path integration algorithm to keep track 12.1). This random walk pattern may be modified to of their homing vector. Path integration means that become straighter (smaller turning angles) in re- foragers continuously update their memory of the sponse to encounters with other ants or lack of vector (direction and distance) to the nest by mea- encounters with food sources, leading the forager suring the directions and distances that they walk. away from the area, or more tortuous (larger turn- In many flying insects, such as bees, distance ing angles), keeping the forager in the vicinity (Gor- moved is measured by visual perception of rate of don 2002). The optimal tortuosity of the search path movement (called optic flow, Srinivasan et al. 2000). is dependent not only on the probable distribution This may play some role in distance measurement of food sources (Fourcassie´ and Traniello 1993), but by ants, but in the ant Cataglyphis it was recently also on the number of cooperative searchers; if demonstrated that a ‘pedometer’ is used; distance is many workers from the same colony are foraging estimated from the number of strides made (Wit- in the same area, foragers should use straighter tlinger et al. 2006, 2007). Direction can be deter- search paths to minimize overlap. Single foragers, mined using a variety of compass systems, such as on the other hand, perform optimally if they use the position of the sun or moon, canopy patterns, a tortuous search path to maximize area coverage prominent landmarks, the direction of wind, or the around the nest without moving too far away, polarization pattern of the blue sky (Collett and which would increase the costs of the return jour- Graham 2004; Ho¨lldobler and Wilson 1990; Mu¨ ller ney (A. Schmolke and A. Dornhaus, unpublished and Wehner 2007). Wood ants (Formica rufa), on the data). These results from modelling studies predict other hand, memorize snapshots of landmarks at that ants from larger colonies may differ from those multiple positions along a route (Collett and Gra- coming from smaller colonies in their search algo- ham 2004). If the ants arrive at a site that matches rithms, a prediction that has yet to be tested empir- their stored view, they can retrieve information on ically. the next landmark, and thus follow their learned

a a

Correlated random walk: new direction is chosen in relation to old one

bc

Figure 12.1 Possible search strategies: (a) systematic search, (b) correlated random walk with large turning angles, and (c) correlated random walk with small turning angles. In a regular random walk, the direction of a step is chosen randomly, independently of the direction of previous movement; in a correlated random walk, step directions are chosen from a distribution centred around the previous direction of movement. FORAGING AND DEFENCE STRATEGIES IN ANTS 215 route back to the nest from any point along it. Main- degree of controversy among researchers. There are taining a library of snapshot landmark memories several possible adaptive explanations for such par- may be cognitively more costly (in terms of neural tial loads, which either focus on the energetic costs tissue or brain capacity required) than a path inte- of transport (Ydenberg and Schmid-Hempel 1994; gration mechanism, but it is also more robust to reviewed in Raine et al. 2006), on the benefits of errors in measurements of distance and direction, recruiting nestmates even at the expense of individ- and it can be used more flexibly if the ant is dis- ual foraging success (Dornhaus et al. 2006a; Roces placed from its location by water, wind, or re- 2002), or on the limitations of the food processing searchers (a condition under which a path chain at the nest (Burd and Howard 2005). integration mechanism fails completely). An even Many of the predictions of optimal forager beha- more costly mechanism of orientation may be to use viour have been derived from modelling studies, a ‘cognitive map’, a map-like representation of the particularly in optimal foraging theory (Raine et al. relative positions of landmarks, the goal (nest or 2006; Ydenberg and Schmid-Hempel 1994). In food source), and the forager’s own position (Col- addition to determining the mathematically opti- lett and Graham 2004). It has been debated for a mal behaviour, however, it is important to quantify long time whether animals in general, and insects in the actual selection pressure or at least the degree to particular, are capable of using cognitive maps, but which such optimization can increase foraging suc- new evidence from honeybees suggests that they cess (Raine et al. 2006). In many cases, cognitively can (Menzel et al. 2006). Such cognitive maps would simpler rules of thumb may work almost equally enable foragers to take novel shortcuts between well. For example, modelling studies predict that sites represented on the mental map, something foragers may optimally return to the nest with a that is impossible if only path integration or route partial rather than a full load in order to collect memories are used. Whether ants use cognitive information at the nest about possible new, superi- maps for orientation or learn routes based on land- or food sources (Dornhaus et al. 2006a). However, marks, it is clear that learning and memory are within a parameter range that is biologically plau- important aspects of foraging (Dornhaus and sible for leaf-cutting ants or honeybees, such partial Franks 2008). Learning also enables workers to re- loads would increase foraging success on an aver- turn to profitable areas at the appropriate time age by a mere 0.000002% (ants) or 1–3% (bees) (Schatz et al. 1999) or to remember previously through this mechanism (Dornhaus et al. 2006a). It found sites for later use or avoidance (Franks et al. is therefore likely that if partial loads are adaptive, 2007b). they evolved for another reason than quicker infor- mation collection by foragers (e.g. faster recruit- ment of other foragers or energetic efficiency, 12.3.4 Load size Roces 2002). An alternative, non-adaptive explana- Once a food source is located, a forager may have to tion is that partial loads simply result from the lack choose the amount of food that it will bring back to of strong selection for maximizing load size. This the nest. It may seem that a forager should always may be the case in taxa that do not incur significant carry as much as possible to make the search trip energetic costs from foraging (see earlier), or if col- worthwhile, and indeed some species seem to ony nutrition is limited by factors other than food tightly match their loads to forager body size (Po- delivery rates. well and Franks 2005), whereas others may use tools to increase their load capacity (pellets of 12.3.5 Morphological adaptations sand functioning as sponges, reviewed in Dornhaus to foraging and Franks 2008). However, it has been observed in several social insects that ‘partial loads’ are some- In addition to potentially finely tuned behavioural times carried back to the nest, in spite of the fact strategies, ants possess a variety of morphological that more food was available at the food source adaptations for capturing and processing food (Roces 2002). This phenomenon has caused some (see Box 12.1) (Carroll 1973; Ho¨lldobler and Wilson 216 ANT ECOLOGY

Box 12.1 Trap-jaw ants Andrew V. Suarez and Joseph C. Spagna The success of ants is often attributed to their used for crushing, impaling, de-limbing, remarkable social behaviour and cooperation. trapping, or ejecting prey or competitors. Group foraging species such as army ants can However, some trap-jaw ants in the recruit hundreds or thousands of individuals to can also use their high-pow- defend, divide, and retrieve resources such as a ered strikes as an escape mechanism; by trig- large insect or even a small vertebrate. How- gering their mandibles against the ground, ever, not all ants are social hunters — some of they can launch themselves several centimetres the most successful predatory ants are solitary into the air in response to threats (Patek et al. hunters. How do they compete with the social 2006) (Figure 12.1.1b). recruiters for resources? One way is by having some of the fastest jaws in the animal king- dom. Evolution and Ecology Of the many remarkable cases of extreme The term ‘trap-jaw ants’ neither describes a feeding ecology in the family Formicidae, few single taxon nor a single clade. In a fascinating rival that of trap-jaw ants (Figure 12.1.1a). example of convergent evolution, trap-jaw These ants use their oversized jaws and asso- morphology has evolved independently at ciated catapult-like muscle-firing ability to least four times in ants, occurring in at least strike prey with extreme speeds and forces — seven genera from three different subfamilies exceeding 60 m/s and 500 times their own body (, , and ) (Fig- weight, respectively (Gronenberg et al. 1993; ure 12.1.1c). The repeated evolution of this Patek et al. 2006). These strikes are typically feeding syndrome makes it an ideal system for

a c

b

start end

Figure 12.1.1 (a) The trap-jaw ant Odontamachus coquereli from Madagascar with its jaws “locked open” and ready to strike. (Photo: Alex Wild). (b) An image sequence of an worker “jumping” with her jaws to escape an attacker. (Image: Patek et al. (2006) Copyright 2006 National Academy of Sciences, USA). (c) Examples of variation in trap-jaw ant morphology. Top row, left to right: , , and (subfamily Myrmicinae); bottom row, left to right: Odontomachus (subfamily Ponerinae) and (subfamily Formicinae). (Photos: www.AntWeb.org.) continues FORAGING AND DEFENCE STRATEGIES IN ANTS 217

Box 12.1 continued

understanding the evolutionary prerequisites mechanism is built using different anatomical for, and ecological correlates of, feeding mor- structures, such as modifications of the jaw phology and mechanics. Trap-jaw ants vary in insertion points in Odontomachus, a modified size from a couple of millimetres (e.g. many labrum in Strumigenys and Daceton, which Strumigenys) to over a centimetre (e.g. some blocks the mandibles from closing, and by in- Odontomachus). They are found in most terlocking mandibular processes in Acanthog- biomes, but are particularly diverse in tropical nathus (Gronenberg 1995; 1996; Gronenberg and subtropical regions. Trap-jaw ants are and Ehmer 1996). In addition to the variation commonly found in litter habitats (such as the in locking mechanisms, the relative size, orien- genera and Strumigenys), but will tation, and attachments of mandible opener also nest arboreally (Daceton and some Odon- and closer muscles vary dramatically across tomachus), and many are ground dwellers liv- trap-jaw ants. Across taxa, the mandible closer ing in a variety of habitats including under muscles can occupy over 60% of the head vol- stones, in rotten logs, and in mounds. ume, and are often contained in visible over- Trap-jaw ants are highly predatory and most sized lobes extending the posterior margins of are dietary generalists, preying upon and the head. Furthermore, variation in muscle scavenging a variety of arthropods. However, volume is accompanied by variation in the rel- some species in the genus Strumigenys appear ative composition of muscle fibre types. For to specialize on springtails, while others in the example, in some trap-jaw ants, the small trig- genus Odontomachus prey predominately on ger muscles that release the strike are among , and a few have even been observed the fastest muscles known in animals (Gronen- harvesting seeds (Brown and Wilson 1959a; berg et al. 1993). Finally, the shapes and sur- Ehmer and Ho¨ lldobler 1995). However, for faces of the jaws themselves vary considerably most trap-jaw ant species, little is known about among species (Figure 12.1.1c). The jaws may their natural history. be long or short, narrow or broad. Many trap- jaws are capped by large medially oriented Morphological and Mechanical Variation terminal teeth, and the leading edges of the Trap-jaw ants show considerable variation mandibles may also be lined with teeth, which both within and among taxa in terms of man- may be sharp or blunt; the leading edges may dible size, shape, and the mechanics of storing also lack teeth and have a wedge- or scissor- and generating force (Figure 12.1.1c). The like surface more suitable for cutting. Whether mandibles are elongated and project from the or not these variations are optimized for cap- head (anteriorly when relaxed, laterally when ture of certain prey-types, colony defence, or cocked), and store energy using a latch or jumping ability is largely unknown and is a rich ‘click’ mechanism. Across trap-jaw species, this area for more research.

1990; Powell and Franks 2005, 2006). Aspects of foraging task (see Plate 10). For example, the leaf- body shape such as relative leg length are likely to cutting ants in the genus Atta produce a range of be adaptations to the specific mode of foraging worker sizes: the largest workers with their strong employed by the respective species; surface-run- mandibles cut leaves, other large workers walk fast ning ants have longer legs, whereas ants that live to transport them, whereas smaller workers tend in an interstitial environment such as leaf litter have fungus inside the nest (Wilson 1980). Morphologi- short legs (Kaspari and Weiser 1999; Kronauer et al. cal differences may also occur interspecifically, pre- 2007b; Scho¨ning et al. 2005; Weiser and Kaspari dicting the diversity and toughness of leaves 2006). Some species also display worker polymor- harvested (Wetterer 1995). Sometimes, very small phism, variation in worker sizes and body shape, workers ride on leaves carried by large workers, producing a worker-caste particularly adapted to a which may have two important defensive functions 218 ANT ECOLOGY

(see Section 12.6.3). Several species also possess species, worker ants improve their trail surface or ‘soldiers’, that is, workers morphologically spe- width by plugging ‘potholes’ with their bodies (Po- cialized for defence (Section 12.6.3). well and Franks 2007) or, more rarely, by forming living bridges (Ho¨lldobler and Wilson 1990). Recent research has shown that in Pharaoh’s ants (Mono- 12.4 Collective strategies in foraging morium pharaonis), foragers can use the trail branch- Ants are eusocial, and collected food is shared ing angles to determine which direction on the trail among all members of the colony. Therefore, for- will lead them back to the nest, and which direction agers do not operate alone, but are part of a colony- will lead out to the food source (trail polarity; Jack- level foraging strategy. There are numerous collec- son et al. 2004). In the same species, it was also tive strategies that are used by different species of found that ants cannot only recruit using phero- ants (Table 12.1). These may include recruitment to mones, but also repel other ants from certain routes, the food source by pheromone trails and a wide for example to indicate unprofitable areas (Robin- variety of other communication signals. son et al. 2005a). Subtle differences in the chemical composition of pheromones may in addition indi- cate who laid them (Jackson et al. 2007). The shape 12.4.1 Recruitment by pheromone trails of the trail system can be species-specific because of differences in these behaviours, or can be an emer- Pheromone trails are the most conspicuous, and gent phenomenon resulting from particular re- therefore the best-studied mode of collective forag- source distributions (Crist and Haefner 1994; ing in ants. Successful ant foragers in many species Edelstein-Keshet et al. 1995; Franks et al. 1991). lay a trail on their way back to the nest, often by intermittent touching or dragging of the gaster on the substrate. Different ant species use different 12.4.2 Recruitment by tandem running glands as sources of recruitment pheromone (Ho¨ll- dobler and Wilson 1990), suggesting possibly many Pheromone trails, however, are not the only mode of independent origins of this behaviour. Pheromone communication available to ants. For example, a well- trails may serve many functions, and not all trails studied recruitment behaviour that involves both serve to find food and retrieve it; other resources, pheromone and mechanical signalsistandemrunning for example nesting sites (Dornhaus et al. 2004), (Mo¨glich and Ho¨lldobler 1974; Plate 12). During a building material (Aleksiev et al. 2007), or mutualist tandem run, an ant worker leads a single recruit to a plants (Webber et al. 2007), are also sought by ants. resource; the recruit follows the leader closely, fre- Furthermore, individual-specific trails may aid in quently touching its antennae to the gaster of the lead- orientation (Ho¨lldobler and Wilson 1990; Masch- ingant.Ifthistouchingisinterrupted,theleadingant witz et al. 1986), or be used to measure area of a will remain in place and wait until the recruit catches nest site (Mallon and Franks 2000). Sometimes per- up. Because of this feedback between leader and fol- manent trunk trails are maintained by ant colonies lower, tandem running may fulfil the criteria for (Edelstein-Keshet et al. 1995), often cleared of vege- ‘teaching’ (Richardson et al. 2007). To initiate a tandem tation or even reinforced with built structures (An- run, the scout ant will use both antennation and a derson and McShea 2001b). In the most extreme ‘tandem calling pheromone’ in the nest (Ho¨lldobler case of the army ants, pheromone trails provide and Wilson 1990; Mo¨glich and Ho¨lldobler 1974). the foundation for an obligate group foraging strat- egy (Rettenmeyer 1963). Ant traffic on trunk trails 12.4.3 Other communication can self-organize into separate traffic lanes, which increases running speed (Couzin and Franks 2003); As these examples show, collective foraging has interactions among ants on the trail may also have mostly been studied in the context of signals in- other functions (Dussutour et al. 2007; Gordon et al. forming recruits about the location of food sources 2008; see Burd 2006 for a review). In some ant or nest sites. However, foragers may communicate FORAGING AND DEFENCE STRATEGIES IN ANTS 219

Table 12.2 Categories of morphological defences seen in ant foragers. See also Plate 13 and Ho¨ lldobler and Wilson (1990: Table 10–3, p. 393f).

Morphological Associated Exemplary defence Function foraging strategies genera References

Armour: Thickened Provides mechanical Common in Cerapachys, Buschinger and exoskeleton, and barriers against predatory species. Nomamyrmex, Maschwitz (1984); sometimes crushing, cutting, Also seen in Paraponera, Ho¨ lldobler and associated with a and puncturing subordinate , Wilson (1990); capsule-like gaster forces exerted by omnivores that , Powell and Clark (expanded first aggressive prey or forage within the Cephalotes (2004) gasteral segment) arthropod enemies territories of (Plate 13) aggressive species Antennal scrobes: Provides sheltered Some predatory and Aconthoponera, Ho¨ lldobler and Depressions or protection for the slave-making Harpagoxenus, Wilson (1990); cavities on the antennae (primary species, as well as Cataulacus, http://www. head that receive sense organs) subordinate Procryptocerus AntWeb.org the antennae when when attacking or omnivores folded under attack Shield: Lateral, Provides expendable Slow-moving Cephalotes, Andersen (2006); de membranous structures that can omnivores, Andrade and expansions of the be seized, chewed, potentially (Plate 13) Baroni-Urbani exoskeleton on the and damaged by foraging within the (1999) head, mesosoma, arthropod enemies territories of or gaster without injury to aggressive, the ant territorial species Erect teeth and May provide Common in relatively Acromyrmex, Buschinger and spines: Sharp mechanical large taxa that Atta, Maschwitz (1984); triangular and protection against forage on Polyrhachis, de Andrade and elongate vertebrate vegetation in the Cephalotes Baroni-Urbani exoskeletal predators (spines understory or (atratus clade) (1999) http:// projections potentially make canopy in the (Plate 13) www.AntWeb.org orientated the ants painful to tropics outwards capture and eat) Decumbent teeth and May provide Widespread, Aconthoponera, Andersen (2006); spines: Lobed, protection against including taxa that Eciton, Buschinger and triangular and arthropod enemies have foraging Phrynoponera, Maschwitz (1984); elongate by blocking direct strategies with Cephalotes, de Andrade and exoskeletal attacks on the high-level Meranoplus, Baroni-Urbani projections main articulation interactions with Harpagoxenus, (1999); http:// orientated along points of the body arthropod enemies Polyrhachis www.AntWeb.org the plane of the and low-level (Plate 13) body and usually interactions with over the main vertebrates articulation points Pubescence: Entire May provide Appears to be Apterostigma, Andersen (2006); body with a dense mechanical barrier associated with Echinopla, http://www. covering of long to biting attack by slow-moving, non- Procryptocerus, AntWeb.org hairs arthropod enemies predatory species Meranoplus (Plate 13) Crypsis: Structures Organic debris Debris camouflage Basiceros, de Andrade and that accumulate conceals the ants. associated with Stegomyrmex, Baroni-Urbani

(Continued) 220 ANT ECOLOGY

Table 12.2 Continued

Morphological Associated Exemplary defence Function foraging strategies genera References

camouflage Exoskeletal ambush predators. Cyphomyrmex, (1999); Diniz and material or create a structures, Outline disrupting Cephalotes Branda˜ o (1993); disrupted body colouration and morphology Ho¨ lldobler and outline hairs may disrupt associated with Wilson (1990); body outlines slow-moving http://www. when ants are omnivores AntWeb.org motionless

other information, such as quality of the resource are common. Pheromone trails can generate a (McCabe et al. 2006; Roces 2002). Communication steep increase in the number of ants recruited with nestmates also influences the decision to start through positive feedback (if recruits add to the foraging: patroller ants may indicate the possible pheromone trail and thus recruit more ants in costs (Greene and Gordon 2007a), and successful turn). However, this effect is dependent on a foraging by others may indicate potential benefits sufficient colony size supplying a large number of leaving the nest (e.g. McCabe et al. 2006). In of potential recruits. In small colonies, pheromone addition, several workers may cooperate to trans- trails may be slow to develop or unstable (Beek- port heavy or unwieldy items to the nest (e.g. man et al. 2001; Edelstein-Keshet et al. 1995). Col- Franks 1987; Traniello and Beshers 1991). These ony size may thus predict the complexity of the ‘teams’ sometimes comprise workers of different communication strategy used where pheromone sizes to maximize transport efficiency (Anderson trails are concerned (Beckers et al. 1989; Herbers and Franks 2001; Franks 1987; Powell and Franks and Choiniere 1996; Mailleux et al. 2003), but it is 2005). Ants may also improve their foraging success less clear whether colony size has an influence on by building new nests or moving existing nests into the benefits of other modes of communication. the proximity of stable resources (van Wilgenburg This is because colony size (i.e. the number of and Elgar 2007). potential recruits at the nest) is irrelevant to the success of a recruitment strategy when the rate of recruitment is not limited by the number of po- 12.4.4 Ecology and evolution of different tential recruits. This is the case whenever each foraging strategies forager can only recruit a fixed number of nest- mates at a time (Dornhaus et al. 2006b), such as in The two factors whose influence on the evolution tandem running or small-group recruitment (inci- of foraging strategies has been studied most are dentally, this is also true for the honeybee waggle spatial resource distribution and colony size. Ants dance). The evolution of group recruitment and that prey on solitary arthropods, which may be tandem running are thus likely to be determined widely distributed across the foraging range and by factors other than colony size. not occur in patches, may have no need for a mass recruitment system (Ho¨lldobler and Wilson 1990). Ants that raid termite colonies, other ant 12.5 Individual defence strategies colonies (i.e. predators, like army ants, or social parasites, like slave-making ants), or that exploit During the act of foraging, individuals use a range other highly profitable, stable resources (e.g. trees of strategies to defend both themselves and any in leaf-cutting ants) on the other hand, are likely resources they are handling. Individual defence to benefit from the ability to recruit nestmates in strategies can thus be broadly defined as any mor- large numbers. In these species, recruitment trails phological, chemical or behavioural characteristic FORAGING AND DEFENCE STRATEGIES IN ANTS 221 used against enemies in such a way that it improves the survival and resource acquisition of individual ants. These defences may, in some cases, involve characteristics used in the foraging process, while others appear to depend on adaptations to the spe- cial dangers of the taxon’s ecology.

12.5.1 Morphological defences

Ant mandibles serve as the primary manipulation- tools in colony life, and they are typically robust and capable of exerting considerable force. The mandibles are therefore of universal importance as defensive weapons, and they are particularly Figure 12.2 Feeding at a rich food resource in effective in taxa with foraging strategies that have Crematogaster and Cephalotes: Crematogaster sp. foragers vigorously defend the food and exude chemical been selected for powerful cutting, crushing, or repellents from the tip of their gasters while a heavily striking mandible morphologies. Good examples armoured Cephalotes persimilis forager pushes past the include the scissor-like mandibles of Atta leaf-cut- Crematogaster sp. defences, apparently without injury. ting ants, the powerful chewing mandibles of Cam- (Photo: Scott Powell) ponotus carpenter ants and the snapping mandibles of predatory genera like Odontomachus (Ho¨lldobler and Wilson 1990; see Box 12.1). trapping camouflage material in some ants, other In addition to morphological weapons, numer- ant taxa have dense covering of long hair that is ous protective morphological structures have kept clean (Table 12.2). These may serve as a me- evolved (Table 12.2; Plate 13). While the general chanical barrier against arthropod enemies, in function of these structures seems clear, their ef- much the same way that plant trichomes provide fectiveness under particular ecological conditions, a mechanical barrier against insect herbivores (e.g. including against specific types of enemies, have Johnson 1975). not been explored in detail. For instance, spines, a In addition to morphological structures that pro- common morphological defence, are often thought vide direct defence, warning colouration (aposema- to provide mechanical protection against verte- tism) may serve as a deterrent to some enemies. In brate predation (Hunt 1983). Direct support for taxa like Pseudomyrmex and , bright and this hypothesis is lacking, but it seems reasonable often patterned colouration would appear to be the for erect spines, particularly as they are common advertisement of their potent sting (see Section in larger taxa that forage on vegetation (Table 12.5.2; Ho¨lldobler and Wilson 1990). In other taxa, 12.2), where predation pressure from birds and the bright colouration may warn of distastefulness. mammals is high. Other taxa, however, have For instance, the gynes and soldiers of numerous lobe-like extensions to the cuticle, teeth, or spines Cephalotes species have brightly coloured gastral that extend backwards over the main articulation eyespots (de Andrade and Baroni-Urbani 1999). points. These structures may protect against ar- Cephalotes lack a functional sting, but some evi- thropod enemies by providing barriers that block dence suggests that many species produce strongly biting attacks on these weak areas. This may be the distasteful chemicals (Coyle 1966; de Andrade and case in army ants, for instance, where backwards- Baroni-Urbani 1999). projecting vertexal lobes or teeth on the head pre- vent direct strikes by their ant prey (S. Powell, 12.5.2 Chemical defences personal observation). Likewise, dense hairs are another common, but poorly understood morpho- A sting mechanism for venom injection is ances- logical defence. While hair can be important for tral (plesiomorphic) in the ants, and remains a 222 ANT ECOLOGY formidable chemical weapon in many extant taxa. (Table 12.2) tend to have limited chemical weap- The sting is formed by the modification of ab- onry. As Hunt (1983) suggested, morphological dominal segments 8–10, and it is fed defensive and chemical defences may therefore represent chemicals from associated glands, with the alternative evolutionary defence strategies, but venom typically produced in the poison gland this idea has yet to be tested. Similarly, robust (Buschinger and Maschwitz 1984). The sting is a analyses of the selective pressures, and particu- particularly conspicuous weapon in predatory larly the foraging strategies, that favour sting species that use it to kill prey, like many poneroid loss have not been conducted. Possible reasons taxa that hunt solitarily (Buschinger and Masch- for sting loss include selection for other types of witz 1984), and group predators like the ‘New chemical weapons that are more effective World army ants’ (Ecitoninae; Powell and Clark against other ants (Buschinger and Maschwitz 2004; Powell and Franks 2005). When threatened, 1984) and an evolutionary shift in diet away these ants also use the sting as a defensive from predation on live arthropods (Kugler weapon. 1979). However, exceptions exist for both of A functional sting has, however, been lost a num- these proposed scenarios. Sting loss is therefore ber of times independently, and the degree to likely to result from a number of interacting which it has been modified, reduced, or co-opted selective pressures. for other functions is also highly varied (Buschinger and Maschwitz 1984). For example, Crematogaster 12.5.3 Behavioural defences produce venom that does not need to be injected. Instead, it is effective when deposited on an enemy, Behaviour can provide unique defence strategies, with the sting little more than an applicator, and it and it can also modify and improve the effective- also acts as a repellent (Buschinger and Maschwitz ness of morphological and chemical defences. 1984; Marlier et al. 2004; Figure 12.2). In other taxa, Bursts of speed are a common behavioural strategy the sting mechanism and associated glands have for avoiding danger in the foraging arena, and path been co-opted for non-defensive functions, as in complexity or tortuosity may also improve the like- Atta, where the poison gland produces only trail lihood of escape (Angilletta et al. 2008). These pheromones (Buschinger and Maschwitz 1984; avoidance strategies are likely to be of the greatest Ho¨lldobler and Wilson 1990). In the more extreme importance in taxa where the foraging strategy has case of the subfamily Formicinae, the sting mecha- selected for high running speeds, such as Catagly- nism has been lost entirely and formic acid, still phis and Ocymyrmex (Hurlbert et al. 2008). Diamet- produced in the poison gland, is deposited or rically opposite to running is the defence strategy of sprayed directly onto enemies (Buschinger and freezing or ‘playing dead’, and it is typically seen in Maschwitz 1984). Finally, in the Dolichoderinae, species with foraging strategies that are associated the sting and poison gland are greatly reduced, with slow movement and morphological defences. and a cocktail of defensive chemicals is instead Examples include Cephalotes (de Andrade and Bar- produced in the pygidial gland (also known as oni-Urbani 1999), Meranoplus (Andersen 2006), and Janet’s gland; Buschinger and Maschwitz 1984). Cyphomyrmex (Ho¨lldobler and Wilson 1990). In the Numerous other glands produce defensive chemi- case of the arboreal genus Cephalotes, body sculp- cals, but these tend to supplement other fighting turing and cryptic colouration may help disrupt the strategies. Examples include foul-smelling and outline of the ants, making them even harder to see repellent secretions produced by the paired man- when they are motionless (Table 12.2; de Andrade dibular glands of many taxa, and sticky meta- and Baroni-Urbani 1999). However, when they vi- pleural gland sections in some Crematogaster sually detect that they have been spotted, or an species (Buschinger and Maschwitz 1984). It is in- enemy strikes at them, they use a radically different teresting to note that taxa with potent chemical strategy: they jump (S. Powell, personal observa- defences often lack strong morphological defences, tion). Recent work has found that once these falling and the most morphologically defended ants ants reach a critical speed, they are capable of FORAGING AND DEFENCE STRATEGIES IN ANTS 223

Box 12.2 The directed aerial descent of arboreal ants Stephen P. Yanoviak The evolution of winged flight in insects is un- Lost workers are costly to ant colonies, and resolved due to a lack of fossil intermediate landing in the unfamiliar understory may have forms, but was likely preceded by directed aerial grave consequences for arboreal ants. Season- descent (i.e. gliding) in an arboreal setting ally flooded forests are common in the tropics (Dudley et al. 2007). Whereas a variety of verte- and present the most extreme circumstances — brates exhibit aerial gliding, the behaviour was fallen insects are immediately consumed by unknown in wingless arthropods until it was surface-feeding fish. But even dry understory recently documented in arboreal ants (Yanoviak litter may pose a significant hazard. For exam- et al. 2005, 2008a). Given that ants are a derived ple, up to 100% of arboreal ants released in the group among insects and are secondarily wing- litter were attacked, and up to 40% were killed less, their gliding behaviour, while interesting by the resident litter fauna in preliminary trials and unexpected, is not directly relevant to the conducted in Peruvian terra firme forest (Ya- origins of winged flight in insects. However, noviak, unpublished data). Thus, the likelihood their abundance in tropical forest canopies, their of a fallen arboreal ant returning to its point of large variation in body size and morphology, origin after landing in the understory is pre- and recent improvements to their phylogenetic sumably low, and gliding reduces this loss (Ya- resolution make ants an excellent focal group for noviak et al. 2005). investigating the selective pressures and aero- Most research on gliding ants to date has dynamic mechanisms associated with this re- focused on the myrmicine genus Cephalotes, markable behaviour. especially the common Neotropical species C. Arboreal ants forage in a relatively exposed atratus (Figure 12.2.1). However, at least six physical setting. They may be accidentally dis- other ant genera include gliding species: Cam- lodged from trees (e.g. Haemig 1997), or may ponotus, Cataulacus, Daceton, Nesomyrmex, voluntarily drop from branches when provoked Procryptocerus, and Pseudomyrmex. Glide per- (Yanoviak and Dudley 2006; Yanoviak et al. formance is generally size-dependent within 2008a). In preliminary studies in Peru, worker and among species (Yanoviak et al. 2005, ants composed 66% of wingless arthropods 2008a). Specifically, smaller workers within co- collected in ten passive funnel traps suspended lonies, and smaller species within genera, tend in the forest canopy (Yanoviak, unpublished to have larger glide indices (glide index = the data). Thus, significant numbers of workers fall horizontal distance travelled per unit vertical as ‘ant rain’ in tropical forests. drop distance). The consistency of these size-

ab

Figure 12.1.2 The Neotropical ant Cephalotes atratus (a) is a common inhabitant of rainforest canopies across South America. If a worker of this species is dislodged from the tree trunk it is able to (b) direct its aerial descent back to the tree trunk. (Photos: Alex Wild) 224 ANT ECOLOGY

Box 12.2 continued

based patterns largely results from basic physics latter two characteristics are necessary for tar- (i.e. smaller ants reach terminal velocity earlier geting during a fall. No nocturnal ants are in a fall). In contrast, mechanisms of aerody- known to glide, and falling C. atratus depend namic stability and glide control are predomi- on visual cues to orient to light-coloured ob- nately behavioural and differ markedly among jects (e.g. lichen-covered tree trunks; Yanoviak taxa. For example, Camponotus workers glide and Dudley 2006). All available evidence indi- toward tree trunks head-first, whereas Cepha- cates that gliding has multiple independent lotes and Cataulacus glide abdomen-first (Ya- origins in ants. Comparative phylogenetic ana- noviak et al. 2005, 2008a). The aerodynamic lyses and more information regarding the relevance of different appendages during a fall ecology, natural history, and morphology of also differs among taxa. Experiments with C. arboreal ants will clarify the selection pressures atratus suggest that the hind legs are necessary associated with the behaviour. for aerodynamic stability in a fall, whereas field In sum, ants provide an excellent model for observations indicate that the forelimbs may studying gliding in small, wingless arthropods serve this function in some Camponotus (Dud- because they are abundant and experimentally ley and Yanoviak, unpubl. data). tractable. However, ongoing research shows Given that not all arboreal ants glide, and not that gliding is not limited to ants — indeed, all ants glide in the same manner, what traits directed aerial descent is widespread among can be associated with this behaviour? Gliding arboreal arthropods, some of which may sup- taxa share four characteristics: (a) costly work- port hypothesized terrestrial origins of insect ers (relatively small colony size and large per- flight (Dudley et al. 2007). Uncovering the me- worker investment); (b) arboreal nesting chanisms and constraints associated with the (ground-nesting arboreal ants like Atta and behaviour in ants will facilitate research on less Paraponera do not glide); (c) good vision; and common taxa that are relevant to understand- (d) diurnal activity (Yanoviak et al. 2005). The ing the evolution of winged flight in insects.

directed descent, returning them to their home tree 12.6.1 Coordinated group defence at the or nearby vegetation with great reliability (Yano- nest viak et al. 2005; Box 12.2). Coordinated group defences are defined here as strategies that use recruitment (pheromonal, tactile, 12.6 Group defence strategies or acoustic) to mobilize a mass defensive response to a specific threat at a specific location. Most ant While individual defences may improve the surviv- species display coordinated group defence when an al and resource acquisition of individual ants, they enemy is detected at the nest, but the strength of the must be put in the broader context of the defensive response and the degree to which a colony relies on strategies of the colony as a whole. These group fight or flight depends on the species, life stage of defences, while benefiting from individual de- the colony, and the enemy. The universal self-sacri- fences, can be defined as those that require coordi- ficing behaviour of ant workers is the key in coordi- nation of more than one individual for success, nated fight responses because it can increase their often at the cost of some of the individuals overall potency. In many taxa, a fight response is involved. The coordinated nature of these collective very general, involving widely broadcast alarm re- actions achieves defensive effectiveness well be- cruitment that releases excitement and aggression yond the sum of the capabilities of the participating (Ho¨lldobler and Wilson 1990). However, these re- individuals. sponses can be more sophisticated, involving FORAGING AND DEFENCE STRATEGIES IN ANTS 225 directed aggression, enemy-specific responses, and nest, and young colonies immediately evacuate cooperative combat strategies. For example, in Oe- without fighting (S. Powell, unpubl. data). Aphaeno- cophylla longinoda, multi-component mandibular gaster colonies, on the other hand, tend to take flight gland secretions act together to alarm workers, at- as soon as a threat is detected, initiating rapid and tract them to a point location, and elicit aggressive highly coordinated evacuation of the entire nest behaviour (Bradshaw et al. 1975). In Pheidole dentata, (Ho¨lldobler and Wilson 1990; Smith and Haight workers recruit nestmates to locations where Sole- 2008). nopsis workers have been detected, but show limit- ed or no response to other potential ant enemies 12.6.2 Coordinated group defence (Wilson 1976). Likewise, Atta species immediately when foraging recruit a massive defensive force when their main invertebrate enemy, the army ant Nomamyrmex In the foraging arena, species with a large work- esenbeckii, is detected, but show no response to force of aggressive workers often recruit a strong other army ants (Powell and Clark 2004). In both defensive force to resources that cannot be har- P. dentata and Atta, the defensive response involves vested by individuals. These species are often re- a special role for soldiers (see Section 12.6.3), and ferred to as ‘extirpators’ (Ho¨lldobler and Wilson Atta also use cooperative combat strategies to 1990) and the resources that they defend may be immobilize army ant raiders. In ant–ant fighting, depleteable, like large prey items, or renewable theory suggests that individual fighting prowess resources like honeydew-producing herbivores and numerical superiority both play key roles in and nectar-producing plants. Examples include the outcome of a battle, and that their relative im- members of the genera Azteca, Camponotus, Crema- portance depends on the type of combat (i.e. a togaster, Pheidole, Solenopsis, and Wasmannia (Ho¨ll- series of one-on-one battles, or an all-against-all dobler and Wilson 1990; McGlynn 2000), with war of attrition) that the battlefield allows (Adams soldiers playing an important role in resource de- and Mesterton-Gibbons 2006; Franks and Partridge fence in Azteca, Solenopsis, and Pheidole (see Section 1993). These predictions have been largely sup- 12.6.3). Collective use of chemical weapons can also ported by observational data from natural large- aid resource defence, both in direct combat with scale battles (Powell and Clark 2004) and from ex- enemies and as repellents around or on a resource perimental studies (McGlynn 2000; Plowes and (Buschinger and Maschwitz 1984). Interestingly, Adams 2005). Further work in this area is likely to however, resource defence is mostly directed prove valuable in understanding the evolution of against other resource-defending species, and is coordinated group fighting strategies in ants, both generally ineffective against morphologically well- at the nest and in the foraging arena. defended foragers or so-called insinuators. Species Flight, or coordinated nest evacuation, is also a of this guild use a combination of stealth and bull- common defensive response in ants. Evacuation dozing tactics to reach and feed at guarded food involves all colony members abandoning the nest (Figure 12.2). It is not known how much food insin- with whatever brood they can carry, and seeking uators can steal from extirpator species in this way, temporary shelter until the threat has passed. In or whether the lost food has any significant fitness some taxa, evacuation is a secondary or simulta- consequences for the extirpators. neous strategy to fighting; in others, often small In a relatively small number of highly aggressive colonies or evacuation specialists, it is the first re- taxa, a territory is established to provide the colony sponse. In all cases, evacuation appears to be par- with exclusive access to resources contained within ticularly important when ants are under attack by the territorial border (reviewed in Ho¨lldobler and army ants, which may occur frequently for ground- Wilson 1990; Traniello 1989). Conspecifics, and nesting taxa in tropical regions (O’Donnell et al. other potential competitors are excluded from the 2007). Thus, while mature Atta colonies fight N. territory with a number of coordinated border de- esenbeckii raiders (Powell and Clark 2004), they re- fence strategies. The first is simply the recruitment sort to evacuation when the army ants enter the of a large number of individuals to defend a border 226 ANT ECOLOGY

Table 12.3 Ant genera with at least one species that has a morphologically and behaviourally specialized soldier caste. List compiled by cross-referencing Baroni-Urbani (1998), Bolton et al. (2006), and Formis 2008 database (Wojcik and Porter 2008).

Ant subfamily Genera with a soldier caste

Aneuretinae Aneuretus Dolichoderinae Azteca, Philidris, Tapinoma Dorylinae Dorylus Ecitoninae Cheliomyrmex, Eciton, Labidus Formicinae Camponotus, Cataglyphis, Cladomyrma, Gesomyrmex, Melophorus, Myrmecorhynchus, Notostigma, Pseudolasius Myrmecinae Acanthomyrmex, Adlerzia, Anisopheidole, Atta, Cephalotes, Carebara, Machomyrma, Monomorium, Orectognatus, Perissomyrmex, Pheidole, Pheidologeton, Solenopsis Pseudomyrmecinae Tetraponera

when a threat is detected, as is the case in Atta misdirected chaos and, in some cases, fighting each (Whitehouse and Jaffe 1996). In species like Azteca other instead of the enemy (Lenoir et al. 2001). Ex- trigona, a substantial presence is permanently main- amples include slave-making species like Formica tained at the border, with reinforcements recruited subintegra and (Lenoir et al. when a threat escalates (Albrecht and Gotelli 2001). 2001), and agro-predators like Gnamptogenys hart- However, full territorial battles can result in mas- mani (Dijkstra and Boomsma 2003). sive mortality on both sides and even colony death (reviewed in Ho¨lldobler and Wilson 1990). In some 12.6.3 Defence, soldiers, and self-sacrifice taxa, this has apparently selected for mechanisms that allow peaceful resolution to territorial dis- Colony defence appears to be a powerful selective putes. For instance, border marking establishes force in the evolution of polymorphism in ants, chemical signals at the territory perimeter that can with numerous independent origins of a soldier be honoured by neighbours to prevent unnecessary caste within the family. A soldier is defined here border skirmishes and escalated aggression (re- as a worker phenotype that is morphologically viewed in Buschinger and Maschwitz 1984; Ho¨lldo- specialized for the role of colony defence. These bler and Wilson 1990). Ritualized combat, on the individuals all display specialized defensive beha- other hand, allows disputes to be resolved by way viours, but they can differ significantly in the de- of a non-destructive show of force: the colony that gree to which their full behavioural repertoire is displays its numerical superiority wins. Ritualized reduced from that of a standard worker. Building combat can take many forms, but includes non- on the list compiled by Baroni–Urbani (1998), and escalating fights (e.g. Cataglyphis niger, Werner adjusting for recent changes in ant , good 1976), ritualized fighting behaviours like front-leg evidence can be found for a soldier caste in 30 boxing (e.g. Camponotus gigas, Pfeiffer and Linsen- genera from 7 subfamilies (Table 12.3). Among mair 2001) and display tournaments (reviewed in these taxa, soldiers can be categorized as Ho¨lldobler and Wilson 1990). specialized for (a) active defence against verte- In discussing coordinated group combat strate- brates, (b) active defence against arthropods, and gies in ants, the special case of repellent and propa- (c) passive defence (i.e. entrance-blocking function) ganda pheromones that have evolved in arms races against arthropods (Ho¨lldobler and Wilson 1990). between ant predators and their ant prey is worth The army ant genus Eciton provides the clearest noting. These chemical weapons, used in a coordi- examples of soldiers specialized for defence against nated group context, neutralize the defensive stra- vertebrates. These soldiers have long mandibles tegies of the victim species by sending them into with recurved tips (Figure 12.3a) that easily FORAGING AND DEFENCE STRATEGIES IN ANTS 227

a puncture vertebrate flesh, but the mandible blades lack grasping surfaces for seizing and cutting ar- thropods (Rettenmeyer 1963). In Eciton species that forage diurnally, like Eciton burchellii and Eciton hamatum, soldiers are deployed at large caches of prey and along foraging trails. In all Eciton species that have a soldier, members of this caste travel in a large group around the queen during emigrations, and remain in significant numbers at the nest at all times (Rettenmeyer 1963; Schneirla 1971). Some of the best examples of soldiers that are effective in active defence against arthropod enemies are seen in Atta and many Pheidole species (Ho¨lldobler and Wilson 1990). A common strategy for soldiers of this type is to dismember their arthropod enemies, which are often other ants, and sometimes this is b achieved with the help of smaller colony members (e.g. Detrain and Pasteels 1992; Powell and Clark 2004; Wilson 1976). Finally, the most striking exam- ples of a soldier caste specialized for passive block- ing defence at the nest are seen in Cephalotes. In the most derived species, the soldier caste has an elab- orate disc-like structure on the head that is used to seal the entrances of the pre-existing arboreal cav- ities inhabited by these ants (Figure 12.3b; de An- drade and Baroni–Urbani 1999; Powell 2008). The basic function of a soldier caste, regardless of type, is clear in most taxa that have one, and one study has clearly demonstrated that the loss of soldiers can dramatically affect colony survivorship (Hase- gawa 1993b). However, remarkably little is under- stood about how the fitness contribution of soldiers Soldiers exhibit a range of defensive Figure 12.3 differs with environmental conditions and their behaviours: (a) Guarding of a foraging trail by a temporal and spatial availability. Studies that ad- soldier in the army ant Eciton hamatum.Thesoldier (right) stands alert as foragers retrieve prey in the dress these types of issues will likely be of great background. When a threat is detected, soldiers run in value in understanding why soldiers are a conver- loops at the site of the alarm and immediately bite gent pattern in the evolution of defence strategies in any vertebrate they encounter. The re-curved tips of ants. the mandibles prevent these soldiers from releasing once they have punctured the flesh of a vertebrate While soldiers represent the common specialized enemy; (b) Entrance blocking by a Cephalotes defensive caste, the so-called hitchhikers provide a persimilis soldier. These soldiers use their heavily unique kind of caste-based defence in Atta. Here, armoured and specialised head-discs to prevent members of the smallest caste (often referred to as enemies from entering the multiple nests of their ‘minims’) ride on leaf fragments being transported colony. Nests are made in pre-existing wood cavities, originally made by wood-boring insects, providing by larger individuals, removing fungal contami- highly defensible structures once soldiers have blocked nants from the harvested leaves (Vieira-Neto et al. the entrances. (Photos: Scott Powell) 2006) and possibly defending transporters against parasitic flies (Feener and Moss 1990; Vieira-Neto 228 ANT ECOLOGY et al. 2006). Adaptations that increase the effective- tural defences can also play a role during foraging. ness of self-sacrificial defence are also not limited to For instance, foragers of Labidus army ants bury soldier evolution. The most notable example is seen large food items (Rettenmeyer 1963), and many in the ‘exploding’ workers of some species in the army ant species build soil tunnels over the stable Camponotus cylindricus clade. These ants have great- foraging trail that is used to deliver prey to the nest ly hypertrophied mandibular glands that stretch (Gotwald 1995). In territorial species, so-called bar- the length of the body. Under conditions of an rack nests housing large numbers of soldiers or extreme threat, muscular contractions rupture the large workers are built near to the border, with glands and the intersegmental membranes so that examples seen in Oecophylla (reviewed in Ho¨lldo- sticky secretions are released explosively onto an bler and Wilson 1990) and Camponotus gigas (Pfeif- enemy. This defence immobilizes the enemy effec- fer and Linsenmair 2001). tively, but kills the ant (Davidson et al. 2007). 12.7 Future directions 12.6.4 Structural defences In exploring the diversity of foraging and defence In addition to the direct defence strategies em- strategies in ants, we have identified a number of ployed by ants, constructed barriers or fortification specific questions that remain unaddressed. How- can play an important role in fending off enemies. ever, in considering future work on these topics, we One of the most basic but common strategies is to would like to highlight two general directions that seal nest entrances with soil or solid objects like we feel are likely to be particularly fruitful. The first stones or twigs. This is seen in a wide range of is a more explicit integration of ecological context taxa, including Atta, Camponotus, Cataglyphis, Har- and environmental variation into empirical studies pegnathus, Messor, and Pogonomyrmex (Buschinger of the efficiency and fitness benefits of foraging and and Maschwitz 1984; Ho¨lldobler and Wilson 1990; defence strategies. The second is the use of modern Powell and Clark 2004). Redundancy may also be comparative analyses to explore the evolutionary built into the nesting behaviour of a species by way relationships between ecology and different strate- of polydomy (two or more spatially separated nests gies. used by one colony). Thus, when one nest is As discussed, the overall efficiency of foraging attacked, the colony may survive because predators strategies in ants can be influenced by numerous do not locate all nests, or because additional nests components, including when to forage, search be- provide a secure destination following evacuation haviour, orientation mechanisms, load selection, of the attacked nest (Debout et al. 2007). In species and morphology. The evolution of each component that have the ability to construct their nest in soil or in any particular taxon may have been influenced using other material, selection is likely to favour by energy budgets (Fewell et al. 1996; Tschinkel some level of defensive architecture. However, 2006; Ydenberg and Schmid-Hempel 1994), mortal- quantitative studies of ant nest architecture are ity risk (Herbers 1981; Nonacs and Dill 1990), com- scarce (Tschinkel 2004), and how architectural com- petitive environment (see references in Dunn et al. ponents may aid defence and increase colony 2007c and Chapter 5), spatial and temporal distri- fitness is essentially unknown. A few peculiar de- bution of resources (e.g. Dornhaus et al. 2006b; fensive nest architectures have been identified, Sundstro¨m 1993; see Chapters 7 and 8), and colony however, with one of the strangest seen in the Neo- size (Anderson and McShea 2001a; Beckers et al. tropical species Blepharidatta conops. These ants con- 1989; Herbers and Choiniere 1996; Ho¨lldobler and struct a highly defensible internal chamber that is Wilson 1990). However, few, if any, empirical stud- separated from the other parts of the nest by a wall ies have explored how the effectiveness of any par- built from insect carcasses. A single entrance hole is ticular foraging strategy component varies under a shaped in the defensive wall, and the queen seals range of realistic ecological conditions that a species the hole with her head, which is morphologically might face. For instance, theory suggests that spa- specialized for the task (Branda˜o et al. 2001). Struc- tial and temporal distributions of resources have FORAGING AND DEFENCE STRATEGIES IN ANTS 229 an important impact on foraging strategies (Dorn- To date, these methods have not been used haus et al. 2006b; Raine et al. 2006). Yet, we have extensively to study the evolution of foraging and very little understanding of how ant foraging stra- defence strategies. However, examples include tegies perform under natural seasonal shifts in re- comparative studies of the evolution of recruitment source distributions and availability or across systems in ants (Baroni-Urbani 1993), the evolution resource gradients within a population. We also of slave-making and the associated propaganda have a very limited understanding of if and how pheromones in the tribe Formicoxenini (Beibl et al. foraging strategies undergo adaptive shifts among 2005; Brandt et al. 2006), strata use and its role in the populations that face distinctly different environ- evolution of forager morphology in Dorylus (Kro- mental conditions. Do decisions on when to forage nauer et al. 2007b; Scho¨ning et al. 2005), the role of shift adaptively across temperature gradients? Do diet in the evolution of a specialized prey-transport orientation mechanisms change with habitat struc- caste in Eciton (Powell and Franks 2006), and the ture? Does the relative use of solitary foraging and role of nesting ecology in the evolution of a recruitment change predictably with different re- specialized soldier caste in Cephalotes (Powell source distributions found at different locations 2008). As knowledge of the evolutionary relation- within a species’ range? Studies that address these ships among ant taxa increases (see Chapter 1), the kinds of questions would be ideal for testing theory power of these kinds of analyses to test new and old that explores how foraging strategies should shift hypotheses on the evolution of foraging and with resource distributions. Similarly, the benefits defence strategies will only increase. The patterns of particular defence strategies relative to particular identified in these studies also have the potential to ranges of environmental conditions, and particular- inform and focus the kinds of empirical studies of ly different kinds of enemies, are very poorly the ecology of foraging and defence strategies that known. Integrated understanding of how the inter- we propose here. actions and benefits of foraging and defence strategies change under different conditions is 12.8 Summary equally rare. We have also highlighted a number of hypoth- Ants and other social insects are model systems eses that seek to explain the evolutionary relation- for the study of foraging strategies, and have ships between environmental conditions and stimulated the development of theories in opti- particular foraging and defence strategies, and the mal foraging, central place foraging, risk and ro- relationships among strategies. For instance, it has bustness, and search algorithms. This is partially been suggested that dietary shifts may explain the due to their abundance and accessibility, and the repeated loss of the sting in ants (Kugler 1979), and ease with which colonies can be studied in the that morphological and chemical defences may be field and in the laboratory; but also due to the alternative trajectories in the evolution of defence fascination exerted by their intricate social beha- strategies (Hunt 1983). These ideas, including those viours. Ant workers may communicate with their new ones suggested by us, are largely based on nestmates or adversaries using a variety of chem- informal surveys of the diversity of foraging and ical, mechanical, visual, auditory, or vibration defence strategies in ants, and have thus not been signals, or multimodal signals and cues, which tested. Modern comparative analyses, which incor- may be specifically directed to single individuals porate information about the evolutionary relation- or used to broadcast information and initiate ships among taxa, provide powerful and robust ‘mass-recruitment’. This diversity in communica- methods for exploring the relationships among tion strategies is mirrored by the diversity of food ecological and phenotypic characters, while sources used, and in the array of defence strate- controlling for the relationships among taxa. The gies that have evolved to improve the acquisition most commonly used methods are those that recon- and retention of resources. Many ants are gener- struct character change over evolutionary time and alists, not only preying on and scavenging a va- test for evolutionary correlations among characters. riety of arthropods, but also using nectar or 230 ANT ECOLOGY honeydew sources where available. However, ferences in diet, as well as differences in habitat there are also many taxa that have become die- structure, competitive environment, and colony tary specialists, feeding on seeds, fungus grown size, have likely led to the broad diversity of in their own gardens, honeydew produced by foraging and defence strategies in ants. Yet, tended hemipterans or nectar produced by muchisstilltobelearntabouttheprocessand plants, and even feeding on other ants. Such dif- patterns that underlie this diversity.