Parallel evolution of thermophilia: daily and seasonal foraging patterns of heat‐adapted desert ants: Cataglyphis and Ocymyrmex species*

In the deserts of northern and southern Africa, respectively, ants of the genera Cataglyphisf oerster (Formicinae) and Ocymyrmexe mery (Myrmicinae) occupy the same ecological niche, which comprises that of a strictly diurnal thermophilic scavenger. Their daily foraging activities exhibit a bimodal pattern in summer and unimodality or complete inactivity in winter. The present study investigates whether these overall patterns are a result of endogenous annual activity rhythms of the colony or are triggered directly by the prevailing ambient temperatures. By exploiting various seasonal temperature regimes and, in particular, by creating near‐nest winter conditions experimentally in summer, it is shown that the latter hypothesis is generally true. However, there are daily and annual variations in the temperature set points at which foraging activities start and finish. These temperatures are lower in the winter than in the summer months and, in summer, they are lower in the morning than in the afternoon. The level of foraging activity in the afternoon reaches maximum values at surface temperatures of 60–63 °C. This means that, in summer months, these thermophilic ants concentrate their foraging activities into a period of almost lethal temperature regimes, during which they have to devote a substantial portion of their time outside the nest to respite (i.e. cooling‐off) behaviour.     

Distribution and comparative morphology of the cloacal gland in ants (Hymenoptera : Formicidae)

The cloacal gland is a paired exocrine structure, which has so far been described only in the formicine species, Camponotus ephippium and Cataglyphis savignyi (Hymenoptera : Formicidae). The gland is formed by 2 clusters of bicellular units with slender duct cells, releasing the glandular secretion through the cloacal membrane. In the present work, a number of ant species, largely of the Formicinae subfamily, have been surveyed for the presence of a cloacal gland. The gland is present in nearly all formicines screened, albeit with a variable development. Cataglyphis, one of the genera with a very prominent cloacal gland, was chosen for a more detailed comparative study. At the ultrastructural level, secretory cells were observed having a well-developed smooth endoplasmic reticulum and Golgi apparatus, typical for pheromone-producing glandular cells. The gland is also present in all dolichoderines screened, but in none of the species of the Aneuretinae, Myrmeciinae, Myrmicinae, Nothomyrmeciinae, or Pseudomyrmecinae investigated. This provides tentative evidence that the cloacal gland is a synapomorphy of the Formicinae and Dolichoderinae, giving support for their hypothesized sister group relationship. Up to now, the function of the cloacal gland remains largely enigmatic.     

Photoresistivity of the cuticle in the gaster segments in the ant species cataglyphis bicolor,messor arenarius and messor semirufus

Changes in the electrical resistance of the cuticle were investigated in the workers of the ant species Cataglyphis bicolor (Formicinae), Messor arenarius and M. semirufus (Myrmicinae). An attempt is made to correlate the photocoductivity of ants to their manner of orientation in the field as individual foragers or by trails.     

Group recruitment in a thermophilic desert ant, Ocymyrmex robustior

Thermophilic desert ants—Cataglyphis, Ocymyrmex, and Melophorus species inhabiting the arid zones of the Palaearctic region, southern Africa and central Australia, respectively—are solitary foragers, which have been considered to lack any kind of chemical recruitment. Here we show that besides mainly employing the solitary mode of food retrieval Ocymyrmex robustior regularly exhibits group recruitment to food patches that cannot be exploited individually. Running at high speed to recruitment sites that may be more than 60 m apart from the nest a leading ant, the recruiter, is followed by a loose and often quite dispersed group of usually 2–7 recruits, which often overtake the leader, or may lose contact, fall back and return to the nest. As video recordings show the leader, while continually keeping her gaster in a downward position, intermittently touches the surface of the ground with the tip of the gaster most likely depositing a volatile pheromone signal. These recruitment events occur during the entire diurnal activity period of the Ocymyrmex foragers, that is, even at surface temperatures of more than 60 °C. They may provide promising experimental paradigms for studying the interplay of orientation by chemical signals and path integration as well as other visual guidance routines.     

Spatio-temporal patterns of colony distribution in monodomous and polydomous species of North African desert ants,genus <Emphasis Type="Italic">Cataglyphis</Emphasis>

Summary Two monogynous species of North African desert ants belonging to the formicine genus Cataglyphis exhibit extremely different habitat preferences, population densities, and population structures. C. fortis is the only Cataglyphis species within the salt-pan flats of the Algerian and Tunisian chotts and sebkhas, whereas C. bicolor, alongside C. albicans and C. ruber, inhabits the nutritionally richer low-shrub semi-deserts surrounding the salt pans. We present a comparative study of the spatio-temporal patterns of colony distribution of the two monogynous species over periods of at least 5 (maximally 15) years. In C. fortis low population densities (0.5 kg body mass per km²) and, correspondingly, large inter-nest distances (40.6 m mean nearest neighbour nest distance) are correlated with absolute intra-annual and high inter-annual nest-site stability (more than 75% inter-annual survival rate) and a monodomous colony structure. In C. bicolor the population density is one hundred times higher (42 kg body mass per km², 9.1 m mean nearest neighbour nest distance), nest-site stability is extremely low in both intra-annual and inter-annual terms (67% intra-annual survival rate for 13-day periods; less than 5% inter-annual survival rate), and polydomy prevails. These marked differences in population structure are discussed with respect to adapted traits such as foraging range, running speed, and relative lengths of the legs.Received 8 August 2003; revised 27 November 2003; accepted 2 December 2003.     

Kompass im Kopf

Ant compass – how desert ants learn to navigate Successful spatial orientation is a daily challenge for many animals. Cataglyphis desert ants are famous for their navigational performances. They return to the nest after extensive foraging trips without any problems. How do ants take their navigational systems into operation? After conducting different tasks in the dark nest for several weeks, they become foragers under bright sun light. This transition requires both a drastic switch in behavior and neuronal changes in the brain. Experienced foragers mainly rely on visual cues. They use a celestial compass and landmark panoramas. For that reason, naïve ants perform stereotype learning walks to calibrate their compass systems and acquire information about the nest's surroundings. During their learning walks, the ants frequently look back to the nest entrance to learn the homing direction. For aligning their gazes, they use the earth's magnetic field as a compass reference. This magnetic compass in Cataglyphis ants was previously unknown.     

Evolution and ecology of directed aerial descent in arboreal ants

Directed aerial descent (DAD) is used by a variety of arboreal animals to escape predators, to remain in the canopy, and to access resources. Here, we build upon the discovery of DAD in ants of tropical canopies by summarizing its known phylogenetic distribution among ant genera, and within both the subfamily Pseudomyrmecinae and the genus Cephalotes. DAD has multiple evolutionary origins in ants, occurring independently in numerous genera in the subfamilies Myrmicinae, Formicinae, and Pseudomyrmecinae. Ablation experiments and video recordings of ants in a vertical wind tunnel showed that DAD in Cephalotes atratus is achieved via postural changes, specifically orientation of the legs and gaster. The occurrence of DAD in Formicinae indicates that the presence of a postpetiole is not essential for the behavior. Evidence to date indicates that gliding behavior is accomplished by visual targeting mediated by the compound eyes, and is restricted to diurnally active ants that nest in trees. Occlusion of ocelli in Pseudomyrmex gracilis workers had no effect on their success or performance in gliding. Experimental assessment of the fate of ants that fall to the understory showed that ants landing in water are 15 times more likely to suffer lethal attacks than are ants landing in leaf litter. Variation in both the aerodynamic mechanisms and selective advantages of DAD merits further study given the broad taxonomic diversity of arboreal ants that engage in this intriguing form of flight.     

Cover Caption

It is often assumed that learning improves foraging, but its direct benefits are not often examined. We demonstrate the contribution of learning to the foraging success of desert ants when a trained colony successfully competes against a naïve one. The outcome also depends on the relative group size. Desert Cataglyphis ants search individually for food (mostly dead prey) without laying pheromone trails (see pages 241-250). The cover photo shows a Cataglyphis niger worker searching for food in its typical sandy habitat. Photo provided Arik Dorfman.     

The hidden spiral: systematic search and path integration in desert ants,Cataglyphis fortis

The main navigational mechanism used by foraging desert ants of the genus Cataglyphis is path integration (dead reckoning). Any such egocentric system of navigation is prone to cumulative navigational errors. Hence, while homing Cataglyphis might have reset its path integration system and yet not arrived at the start of its foraging excursion, the nest entrance. Then it resorts to piloting or performs a systematic search for the nest. The search pattern consists of a system of loops of ever increasing size centred about the origin, i.e. the start of the search. Here we show that underlying the system of loops is a spiral search programme that gets transformed into the observed pattern of loops by the ant's idiosyncratic path-integration algorithm. The ant starts to follow a spiral course, then breaks off this course and walks towards the centre, i.e. to what its path-integration system has computed to be the origin of the search. This reset episode is followed by another spiral course, which is terminated by the next reset, and so forth. After each reset, the spiral gets wider, so that the whole pattern expands. Futhermore, every now and then the spiral might change its sign. Computer simulations based on these simple rules lead to search patterns of the kind actually recorded in Cataglyphis ants. These patterns ensure that those parts of the area in which the target (nest entrance) is most likely to be located are searched most heavily; in other words: the search density profile is adapted to the probability density function of the target.     

Use of Long-Term Stored Vector Information in the Neotropical Ant <Emphasis Type="BoldItalic">Gigantiops destructor</Emphasis>

We investigated how the formicine ant Gigantiops destructor can use vector information to navigate within the cluttered environment of the rain forest. Displaced foragers use skylight information to move in the theoretical feeder-to-nest direction, whether they are prevented from updating their path-integrator during foraging or captured at the departure from their nest, i.e. with a current accumulator state very close to zero. Only ants that have collected food are able to download a long-term stored reference vector pointing in the nest direction, irrespective of the current accumulator state of their path-integrator stored in a working memory and independent of familiar landmarks. Depending on the release sites, ants that became lost at a maximum distance of 50 cm could still hit and recognize their familiar route, or they engaged in a systematic search for it centered on the release sites. In contrast to Cataglyphis desert ants, Gigantiops ants do not rely primarily on the current accumulator state of their egocentric path integrator. Such a long-term vector-based navigation primed by food capture is well adapted for a tropical ant foraging during periods spanning several hours. This could prevent the numerous cumulative errors in the evaluation of the angles steered that might result from a continuously running path-integrator operating during complex foraging patterns performed at ground or arboreal levels and during passive displacement in response to heavy rain.     

PCR primers for polymorphic microsatellite loci in the facultatively polygynous plant‐ant Petalomyrmex phylax (Formicidae)

Fourteen microsatellite loci were isolated and their level of polymorphism characterized in two populations of the facultatively polygynous plant‐ant Petalomyrmex phylax (Formicinae). High levels of within‐population variation were observed at most loci, with number of alleles ranging from two to 15, and heterozygosity from 0.050 to 0.925. Cross‐species amplification of these loci was also tested in four plant‐ant species belonging to three other genera, Aphomomyrmex, Cladomyrma (both Formicinae) and Cataulacus (Myrmicinae).     

Differences in Forage-Acquisition and Fungal Enzyme Activity Contribute to Niche Segregation in Panamanian Leaf-Cutting Ants

The genera Atta and Acromyrmex are often grouped as leaf-cutting ants for pest management assessments and ecological surveys, although their mature colony sizes and foraging niches may differ substantially. Few studies have addressed such interspecific differences at the same site, which prompted us to conduct a comparative study across six sympatric leaf-cutting ant species in Central Panama. We show that foraging rates during the transition between dry and wet season differ about 60 fold between genera, but are relatively constant across species within genera. These differences appear to match overall differences in colony size, especially when Atta workers that return to their nests without leaves are assumed to carry liquid food. We confirm that Panamanian Atta specialize primarily on tree-leaves whereas Acromyrmex focus on collecting flowers and herbal leaves and that species within genera are similar in these overall foraging strategies. Species within genera tended to be spaced out over the three habitat categories that we distinguished (forest, forest edge, open grassland), but each of these habitats normally had only a single predominant Atta and Acromyrmex species. We measured activities of twelve fungus garden decomposition enzymes, belonging to the amylases, cellulases, hemicellulases, pectinases and proteinases, and show that average enzyme activity per unit of fungal mass in Atta gardens is lower than in Acromyrmex gardens. Expression profiles of fungal enzymes in Atta also appeared to be more specialized than in Acromyrmex, possibly reflecting variation in forage material. Our results suggest that species- and genus-level identities of leaf-cutting ants and habitat-specific foraging profiles may give predictable differences in the expression of fungal genes coding for decomposition enzymes.     

Spatio‐temporal patterns and interactions with honeydew‐producing Hemiptera of ants in a Mediterranean citrus orchard

• 1 The role of ants in the citrus agro‐ecosystem is controversial and understanding their ecology may help to clarify their function. The present study determined the daily and seasonal foraging patterns, the spatial distribution, the feeding sources and the associations with honeydew‐producing Hemiptera of three ant species that forage in citrus canopies.
• 2 The dominant ants Pheidole pallidula (Nylander) (Myrmicinae) and Lasius grandis Forel (Formicinae) foraged in mutually exclusive territories within the field, although they both shared their territory with the subordinate Plagiolepis schmitzii Forel (Formicinae), a distribution pattern known as ‘ant mosaic’.
• 3 The observed mean overlap for the spatial distribution was significantly lower than the generated by null models, providing strong evidence of spatial interspecific competition, especially between the two dominants.
• 4 Ants ascended to the canopies from April until November. Colony nutritional requirements and temperature probably shape their seasonal foraging patterns. The daily activity pattern of P. schmitzii was strictly diurnal, whereas L. grandis and P. pallidula were active during the entire day.
• 5 The ants' diet in the canopies consisted principally of hemipteran honeydew, whereas citrus nectar and predation/scavenging did not represent important food sources. More than 60% of the total honeydew sources and 100% of the citrus mealybug Planococcus citri colonies were tended by ants during spring and summer.

     

Notes on the ant genus Cataglyphis Foerster, 1850 (Hymenoptera,Formicidae) in the Arabian Peninsula with description of a new species and a key to species of the C. pallida-group

Cataglyphis fisheri sp. n. is described and illustrated from the United Arab Emirates, Oman and Kingdom of Saudi Arabia based on the worker caste. It belongs to the Cataglyphis pallida-group which is recorded for the first time from the Arabian Peninsula. Cataglyphis fisheri sp. n. is similar to Cataglyphis pallida Mayr, 1877 from Kazakhstan. Differential diagnosis between these two species is given and a key to the species of the Cataglyphis pallida-group is presented. Cataglyphis laylae Collingwood, 2011 is treated as a junior synonym of Cataglyphis saharae Santschi, 1929. Cataglyphis flavobrunnea Collingwood & Agosti, 1996 is redescribed and a lectotype for this species is designated.     

Excessive sulphur accumulation and ionic storage behaviour identified in species of Acacia (Leguminosae: Mimosoideae)

Background and Aims Thiophores, which are typically desert gypsophytes, accumulate high (2–6 % S dry weight) sulphur concentrations and may possess unique tolerance to environmental stress factors, e.g. sulphate/metal toxicity, drought and salinity. Little is known of the prevalence of the behaviour or the associated physiological aspects. The aim of this study was to (a) determine the prevalence of thiophore behaviour in a group of Australian xerophytes; (b) identify elemental uptake/storage characteristics of these thiophores; and (c) determine whether the behaviour is constitutive or environmental.Methods The elemental composition of soils and the foliage of 11 species (seven genera) at a site in the Tanami Desert (NT, Australia) was compared and 13 additional Acacia species from other locations were examined for elevated calcium and sulphur concentrations and calcium–sulphur mineralization, thought to be particular to thiophores.Key Results Acacia bivenosa DC. and 11 closely related species were identified as thiophores that can accumulate high levels of sulphur (up to 3·2 %) and calcium (up to 6.8 %), but no thiophores were identified in other genera occupying the same habitat. This behaviour was observed in several populations from diverse habitats, from samples collected over three decades. It was also observed that these thiophores featured gypsum (CaSO₄·2H₂O) crystal druses that completely filled cells and vascular systems in their dried phyllode tissues.Conclusions The thiophores studied exhibit a tight coupling between sulphur and calcium uptake and storage, and apparently store these elements as inorganic salts within the cells of their foliage. Thiophore behaviour is a constitutive trait shared by closely related Acacia but is not highly prevalent within, nor exclusive to, xerophytes. Several of the newly identified thiophores occupy coastal or riparian habitats, suggesting that the evolutionary and ecophysiological explanations for this trait do not lie solely in adaptation to arid conditions or gypsiferous soils.     

A neurotoxic pesticide changes the outcome of aggressive interactions between native and invasive ants

Neurotoxic pesticides, such as neonicotinoids, negatively affect the cognitive capacity and fitness of non-target species, and could also modify interspecific interactions. We tested whether sublethal contamination with neonicotinoid could affect foraging, colony fitness and the outcome of behavioural interactions between a native (Monomorium antarcticum) and an invasive ant species (Linepithema humile). The foraging behaviour of both ants was not affected by neonicotinoid exposure. Colonies of the invasive species exposed to the neonicotinoid produced significantly fewer brood. In interspecific confrontations, individuals of the native species exposed to the neonicotinoid lowered their aggression towards the invasive species, although their survival probability was not affected. Exposed individuals of the invasive species interacting with non-exposed native ants displayed increased aggression and had their survival probability reduced. Non-exposed individuals of the invasive species were less aggressive but more likely to survive when interacting with exposed native ants. These results suggest that non-target exposure of invaders to neonicotinoids could either increase or decrease the probability of survival according to the exposure status of the native species. Given that, in any community, different species have different food preferences, and thus different exposure to pesticides, non-target exposure could potentially change the dynamics of communities and influence invasion success.     

Desert ants: is active locomotion a prerequisite for path integration?

Desert ants Cataglyphis fortis have been shown to be able to employ two mechanisms of distance estimation: exploiting both optic flow and proprioceptive information. This study aims at understanding possible interactions between the two possibly redundant mechanisms of distance estimation. We ask whether in Cataglyphis the obviously minor contribution of optic flow would increase or even take over completely if the ants were deprived of reliable proprioceptive information. In various experimental paradigms ants were subjected to passive horizontal displacements during which they perceived optic flow, but were prohibited from active locomotion. The results show that in desert ants active locomotion is essential for providing the ants’ odometer and hence its path integrator with the necessary information.     

Phylogenetic relationships between the slave‐making ants Rossomyrmex and their Proformica hosts in relation to other genera of the ant tribe Formicini (Hymenoptera: Formicidae)

The ant genus Proformica is very common to Eurasian semi‐deserts, and a few species are parasitized by the slave‐making ants Rossomyrmex. However, the phylogenetic relationship between Proformica (host) and Rossomyrmex (parasite) remains unclear as another closely related genus (Cataglyphis) could be a sister group of Rossomyrmex. This work has two main goals: (i) to study the phylogenetic relationships among Proformica, Rossomyrmex, and other genera of the tribe Formicini, with a special focus on the highly diverse genus Cataglyphis; and (ii) to reconstruct the biogeographical distribution of parasite and host genera. We perform a phylogenetic study for the first time including several species of the genera Rossomyrmex, Proformica, and Cataglyphis. Our results indicate that Proformica and Rossomyrmex are reciprocally monophyletic and that Rossomyrmex is nested within Cataglyphis, rendering the latter paraphyletic. Finally, the ancestral distribution range of the host genus could be situated in Central Asia and subsequently dispersed to Western Europe, whereas additional studies are required to clarify the range of the parasite.     

Worker thermal tolerance in the thermophilic ant Cataglyphis cursor (Hymenoptera, Formicidae)

In the thermophilic ant genus Cataglyphis, species differing in their physical caste system have developed alternative mechanisms to face extreme heat by physiological and/or behavioural adaptations. In this study, we tested whether thermal tolerance is related to worker size in the ant Cataglyphis cursor that presents intermediate worker size compared with previously studied species (size range 3.5–10 mm). Thermal tolerance at two temperatures was tested in the laboratory on colonies originating from two habitats (seaside versus vineyard), known to differ in average worker size. As expected large workers were more resistant to high temperature than small workers, but the effect of worker size on thermal resistance was less pronounced under the more extreme temperatures. The pattern of thermal tolerance was similar in the two habitat types. After controlling for worker size, worker thermal tolerance significantly varied amongst colonies, but this variation was not related to colony size. Our results suggest that a higher thermal tolerance can confer an advantage to larger workers especially during foraging and are discussed in the context of the evolution of worker size in ants.     

Multiple mating and supercoloniality in Cataglyphis desert ants

In social organisms, the breeding system corresponds to the number of breeders in a group, their genetic relationships, and the distribution of reproduction among them. Recent, genetically based studies suggest an amazing array of breeding system and reproductive strategies in desert ants of the genus Cataglyphis. Using highly polymorphic DNA microsatellites, we performed a detailed analysis of the breeding system and population genetic structure of two Cataglyphis species belonging to the same phylogenetic group: C. niger and C. savignyi. Our results show that both species present very different breeding systems. C. savignyi colonies are headed by a single queen and populations are multicolonial. Remarkably, queens show one of the highest mating frequency reported in ants (M_p = 9.25). Workers can reproduce by both arrhenotokous and thelytokous parthenogenesis. By contrast, colonies of C. niger are headed by several, multiply mated queens (M_p = 5.17), and they are organized in supercolonial populations made of numerous interconnected nests. Workers lay arrhenotokous eggs only. These results illustrate the high variability in the socio‐genetic organization that evolved in desert ants of the genus Cataglyphis. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 866–876.