Ant‐following and the prevalence of blood parasites in birds of African rainforests

Blood parasites are widespread in birds, several are pathogenic and may affect the fitness of their hosts, and their evolution. By reanalyzing recently published data I show that parts of the variation in prevalences of parasites in the blood of African rainforest birds and the occurrence of similar or same parasite haplotypes in rather unrelated birds are well understood when considering the ecological aspects of foraging of some of these birds. Specialized ant‐following birds, which regularly follow the massive swarm raids of army ants and feed on insects flushed by the ants, have higher prevalences of nematode microfilariae (~10×), Trypanosoma (~10×), and Plasmodium parasites (~2×) and a much higher probability of infection with multiple parasites than other birds. Moreover, birds regularly attending army ant swarms share identical Trypanosoma haplotypes and show genetically similar microfilariae haplotypes. I conclude that ant‐following increases the probability of birds to get infected with blood parasites and may facilitate the switch of a parasite species from one host species to another. The costs of higher parasite intensities involved when specializing on following ant swarms may have influenced the evolution of foraging behaviour in birds of African rainforests and may help to explain the relatively low number of specialized ant‐following bird species on the African continent.     

Birds and army ants in a fragment of the Atlantic Forest of Brazil

ABSTRACT Little is known about the birds associated with army‐ant swarms in the Brazilian Atlantic forest. Our objectives were to locate and monitor army‐ant swarms in the Atlantic rainforest of Brazil and to identify the species of birds that attended the swarms and exhibited bivouac‐checking behavior. From July 2004 to August 2005, we located 49 swarms of army ants, including 28 Eciton burchelli, 19 Labidus praedator, and 2 Eciton vagans swarms. No birds were present at 17 (35%) swarms. At 32 swarms where birds were present, 22 (69%) were E. burchelli swarms and 10 (31%) were L. praedator swarms. No birds were observed at the two E. vagans swarms. We identified 66 species of birds attending the swarms, but only 43 species were observed foraging on prey flushed by the ants. Eighteen of these species had not been previously reported to forage in association with army‐ant swarms. Most birds observed during our study attended army‐ant swarms opportunistically, with White‐shouldered Fire‐eyes (Pyriglena leucoptera) the only obligate ant follower. Our observations suggest that the arthropods and other organisms flushed by army ants represent an important food resource for several species of birds in the Atlantic forest ecosystem.     

Microclimatic factors associated with elevational changes in army ant density in tropical montane forest

Abstract.  1. The density (rate of encountering foraging raids) and species richness of army ants (Formicidae: Ecitoninae, and behaviourally convergent Ponerinae) was measured in montane tropical forest. Above-ground and subterranean army ant raids were sampled using standard protocols at four sites across an elevational gradient (1200–1650 m above mean sea level) in and near cloud forest in the area of Monteverde, Costa Rica.
2. Mean ambient temperature differed among sites, and decreased with elevation. For the above-ground foraging army ant species, raid rates also declined with elevation. Surface army ant raid rates, however, were not affected by day to day weather variation within sites (temperature, cloud cover, or precipitation).
3. For the underground foraging army ant species, raid rates did not vary directionally with elevation, and subterranean raid rates were not affected by day to day weather variation within sites.
4. Army ant species richness was not directionally related to elevation, and species sharing among sites was generally high.
5. Army ant community structure changes with elevation in Neotropical montane forest, and the results suggest that the strongest effects are of temperature regimes on the density of raids. These findings provide a baseline against which to detect changes in army ant communities that may accompany directional climate change in tropical cloud forests.     

Army ants in four forests: geographic variation in raid rates and species composition

1. The New World army ants are top predators in the litter of tropical forest, but no comprehensive studies exist on variation in assemblage-wide activity and species composition. We used standardized protocols to estimate foraging raid rates and species composition of army ant communities in four Neotropical forests. The study sites spanned approximately 10 degrees latitude, with two sites each in Central and South America. 2. We recorded a total of 22 species of army ants. The four sites varied in observed and estimated species richness. Species overlap was highest between the Central American sites, and lowest between the South American sites. 3. Raid activity varied significantly among sites. Raid activity per kilometre of trail walks was over four times higher at the most active site (Sta. Maria, Venezuela) than at the least active site (Barro Colorado Island, Panama). Furthermore, each site showed a different diel pattern of activity. For example, raid activity was higher during daylight hours in Costa Rica, and higher at night in Venezuela. Raid activity relationships with ambient temperature also varied significantly among sites. 4. The overall rate of army ant raids passing through 1 m(2) plots was 0.73 raids per day, but varied among sites, from 0 raids per day (Panama) to 1.2 raids per day (Venezuela). 5. Primarily subterranean species were significantly more abundant in Venezuela, and above-ground foragers that form large swarm fronts were least abundant in Panama. The site heterogeneity in species abundance and diel activity patterns has implications for army ant symbionts, including ant-following birds, and for the animals hunted by these top predators.     

Elevational and geographic variation in army ant swarm raid rates

Geographic and elevational variation in the local abundance of swarm-raiding army ants has implications for the population dynamics of their prey, as well as affecting the profitability of army-ant-following behavior for birds. Here, we analyze systematically collected data on E. burchellii and L. praedator raid rates from geographically and elevationally wide-ranging sites, from lowland to montane forests. We show that raids of each species, and of both species pooled, reach peak densities at intermediate (premontane) elevations. These patterns suggest that army ant swarm raids are relatively abundant in Neotropical montane forests. Therefore, a paucity of ant raids does not explain the absence of obligate ant-following bird species, particularly true antbirds (Thamnophilidae), from montane forests. As army ant raids are relatively common at middle elevations, opportunities exist for other montane bird taxa to exploit army ant raids as a food source.     

The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants

The unique nomadic life-history pattern of army ants (army ant adaptive syndrome), including obligate colony fission and strongly male-biased sex-ratios, makes army ants prone to heavily reduced effective population sizes (N _e). Excessive multiple mating by queens (polyandry) has been suggested to compensate these negative effects by increasing genetic variance in colonies and populations. However, the combined effects and evolutionary consequences of polyandry and army ant life history on genetic colony and population structure have only been studied in a few selected species. Here we provide new genetic data on paternity frequencies, colony structure and paternity skew for the five Neotropical army ants Eciton mexicanum, E. vagans, Labidus coecus, L. praedator and Nomamyrmex esenbeckii; and compare those data among a total of nine army ant species (including literature data). The number of effective matings per queen ranged from about 6 up to 25 in our tested species, and we show that such extreme polyandry is in two ways highly adaptive. First, given the detected low intracolonial relatedness and population differentiation extreme polyandry may counteract inbreeding and low N _e. Second, as indicated by a negative correlation of paternity frequency and paternity skew, queens maximize intracolonial genotypic variance by increasingly equalizing paternity shares with higher numbers of sires. Thus, extreme polyandry is not only an integral part of the army ant syndrome, but generally adaptive in social insects by improving genetic variance, even at the high end spectrum of mating frequencies.     

The largest animal association centered on one species: the army ant <Emphasis Type="Italic">Eciton burchellii</Emphasis> and its more than 300 associates

As possibly two of the last true naturalists, Carl Rettenmeyer and his wife Marian dedicated their lives to the study of army ants and their associates. Over the course of 55 years, the Rettenmeyers went on numerous field trips mainly to the Central American tropics and analyzed hundreds of self-collected samples and those sent by a multitude of other scientists, who were inspired by Carl’s enthusiasm. It comes as no surprise that Carl Rettenmeyer became the world’s leading expert on army ant associates. This paper, which the Rettenmeyers nearly completed before Carl’s death in 2009, gives the first comprehensive list of animals known to be found in the company of a single army ant species: Eciton burchellii. The 557 recorded associates range from birds to insects and mites and comprise the largest described animal association centering around one particular species. Although some of these associates may be opportunistic encounters, we are confident that approximately 300 of the recorded species depend on the ants, at least in part, for their existence. The extinction of E. burchellii from any habitat over its vast area of distribution is likely to cause the extinction of numerous associated animals at that site. This overview will hopefully inspire researchers throughout the world to follow in the Rettenmeyers’ footsteps and continue the investigation of army ants and their associates.     

Vertebrate Fruit Removal and Ant Seed Dispersal in the Neotropical Ginger Renealmia alpinia (Zingiberaceae)*

Plants frequently display fruit characteristics that support multiple seed‐dispersal syndromes. These ambiguous characteristics may reflect the fact that seed dispersal is usually a complex process involving multiple dispersers. This is the case for the Neotropical ginger Renealmia alpinia (Zingiberaceae). It was originally suggested that the aromatic fruits of R. alpinia located at the base of the plant are adapted for terrestrial mammal seed dispersal. However, the dark‐purple coloration of the fruits and bright orange aril surrounding the seeds suggest that birds may play a role in R. alpinia seed dispersal. At La Selva Biological Station, Costa Rica, we used camera traps to record vertebrate visits to infructescences of R. alpinia. Most visitors were toucans and aracaris (Ramphastidae). However fruits were also removed by terrestrial mammals (coatis and armadillos). In addition to vertebrate fruit removal, some of the fruits dehisce and the seeds that fall on the ground are dispersed by ants. Fruitfall traps showed that 77 percent of fruits are removed by vertebrates. However, 15 percent of fruits fall to the base of parent plants to be potentially dispersed by ants. Experiments using a laboratory ant colony showed that ants are effective seed dispersers of R. alpinia. Ant seed manipulation increased germination success and reduced time to germination. In conclusion, primary seed dispersal in the Neotropical ginger R. alpinia is mostly performed by birds, additionally ants are effective dispersers at short distances. Seed dispersal in R. alpinia is a complex process involving a diverse array of dispersal agents.     

Serial monodomy in ants: an antipredator strategy?

Abstract.  1. The term serial monodomy is used to describe a life-history phenomenon in social insects. Serially monodomous colonies maintain multiple nests for their exclusive use, but only occupy one nest at a time.
2. The hypothesis that colony odours mediate nest relocation decisions was tested in the serially monodomous species Aphaenogaster araneoides from Central America. Odour extracts of colony members were created using a non-polar solvent.
3. Colonies strongly avoided reoccupying nests treated with colony odour extracts, while control colonies often returned to nests subjected to solvent-only control. Behavioural observations indicated that A. araneoides colonies are capable of detecting army ant ( Eciton burchellii ) raids up to 1.4 m from the raiding front, with several seconds to evacuate nests.
4. It is proposed that the function of serial monodomy in A. araneoides is the reduction of nest odour to enhance detection of predaceous army ants. Serial monodomy may be a widespread but undocumented mode of nesting where army ants occur in tropical and subtropical climates.     

Specializations of birds that attend army ant raids: An ecological approach to cognitive and behavioral studies

Tropical birds forage at army ant raids on several continents. Obligate foraging at army ant raids evolved several times in the Neotropical true antbird family (Thamnophilidae), and recent evidence suggests a diversity of bird species from other families specialize to varying degrees on army ant exploitation. Army ant raids offer access to high prey densities, but the ant colonies are mobile and widely spaced. Successful army ant exploitation requires solving a complex foraging problem because army ant raids are unpredictable in space and time. Birds can counteract the challenges posed by the ants by using strategies that raise their chances of detecting army ant raids, and birds can use additional strategies to track army ant colonies they have located. Some features of army ant biology, such as their conspicuous swarms and columns, above-ground activity, and regular cycles of behavior, provide opportunities for birds to increase their effectiveness at exploiting raids. Changes in sensory, cognitive and behavioral systems may all contribute to specialized army ant exploitation in a bird population. The combination of specializations that are employed may vary independently among bird species and populations. The degree of army ant exploitation by birds varies geographically with latitude and elevation, and with historical patterns such as centers of distribution of obligate thamnophilid antbirds. We predict the set of specializations a given bird population exhibits will depend on local ecology, as well as phylogenetic history. Comparative approaches that focus on these patterns may indicate ecological and evolutionary factors that have shaped the costs and benefits of this foraging strategy. The development of army ant exploitation in individual birds is poorly understood, and individual expression of these specializations may depend on a combination of genetic adaptation with cognitive plasticity, possibly including social and experiential learning. Future studies that measure developmental changes and quantify individual differences in army ant exploitation are needed to establish the mechanisms underlying this behavior.     

Complex Nesting Behavior by Two Neotropical Species of the Ant Genus Stenamma (Hymenoptera: Formicidae)1

Two Neotropical ant species, Stenamma expolitum Smith and S. alas new species (described here), exhibit three unusual nesting behaviors: (1) they build architecturally sophisticated nest entrances that elevate the nest opening away from the surface; (2) they maintain multiple identical nests but occupy only one of them; and (3) they keep a round “door pebble” at the nest entrance, with which they plug the opening in response to army ants. Adaptive hypotheses for these behaviors are discussed, including the possibility that there are multiple lines of defense against army ant predation.     

Pollination of Richea dracophylla (Ericaceae) and the role of the nocturnal ant Notoncus hickmani (Formicinae)

Our observation of large numbers of ants Notoncus hickmani (Formicinae) on the flowers of a Tasmanian endemic shrub Richea dracophyllum (Ericacea) during the night in winter prompted us to carry out a more extensive study of pollination of R. dracophyllum at two sites. Terminal panicles bear inflorescences of 300+ flowers whose petals are fused into calyptrae covering the reproductive organs, and the calyptrae must be removed before pollination can occur. To exclude birds, we placed mesh bags over some inflorescences. Inflorescences with exclusion bags had a high proportion of retained calyptra and the numbers of viable seeds were greatly reduced. We found R. dracophyllum to have a very long flowering period (more than 6 months) and a range of floral visitors, including honey-eaters (Meliphagidae) and flying insects. At one site we observed large numbers (up to 100) of N. hickmani on inflorescences between dusk and midnight during winter at air temperatures down to 2.5°C. They fed on nectar from flowers that had lost their calyptra where they were exposed to pollen from the anthers and scanning electron microscopy showed high numbers of pollen grains being carried on the ants. The feeding behaviour of these ants would facilitate pollination between adjacent flowers (geitonogamy). Smaller numbers of dolichoderine ants (Iridomyrmex bicknelli?) were observed during the daytime in spring but mainly fed under partially detached calyptrae where they had little exposure to pollen. We suggest that R. dracophylla is pollinated by a range of species and functional groups—birds, flying insects and ants, and that the pollinating species will vary during the year and between sites, although insects depend on birds to remove the calyptrae. Ant pollination is rare, nocturnal ant pollination is extremely rare, and pollination by nocturnal cryophilic ants has not been documented previously.     

Ornithophilous canopy species in the Atlantic rain forest of southeastern Brazil

ABSTRACT.   In tropical ecosystems, birds play a relevant role in plant reproduction. Although hummingbirds are regarded as the most important vertebrate pollinators in the Neotropics, the possible role of perching birds as pollinators has been neglected. From 2003 to 2005, we observed 68 species of plants visited by birds in an Atlantic rainforest in southeastern Brazil, including three canopy species: Spirotheca rivieri (Malvaceae, Bombacoidea), Schwartzia brasiliensis (Marcgraviaceae), and Psittacanthus dichrous (Loranthaceae). Flowers of these three species were visited by 15 different species of perching birds and by hummingbirds. The flowers of these three plants are colorful, ranging from deep red or purple to orange. Spirotheca rivieri blooms during the austral winter and Schwartzia brasiliensis during the summer. The flowers of these two species produce copious amounts of dilute nectar in easily accessible structures and both species appear to depend primarily on perching birds as pollinators, with hummingbirds being secondary or minor pollen vectors. The tubular, narrow flowers of P. dichrous are produced during the austral summer and are visited primarily by hummingbirds. Perching birds also visit the flowers, but destroy them. Our results suggest that previous estimates of the number of perching birds that feed on nectar may be too low and that flowers pollinated by perching birds may be more common in the canopy of Neotropical forests than previously thought.     

Effects of aphids on foliar foraging by Argentine ants and the resulting effects on other arthropods

Abstract.  1. Although interactions between ants and honeydew-producing insects have received considerable study, relatively little is known about how these interactions alter the behaviour of ants in ways that affect other arthropods. In this study, field and greenhouse experiments were performed that examined how the presence of aphids ( Aphis fabae solanella ) on Solanum nigrum influenced the foraging behaviour of Argentine ants ( Linepithema humile ) and, in turn, modified the extent to which ants deter larval lacewings ( Chrysoperla rufilabris ), which are known aphid predators.
2. A field experiment demonstrated that the level of foliar foraging by ants increased linearly with aphid abundance, whereas no relationship existed between the level of ground foraging by ants and aphid abundance.
3. In the greenhouse, as in the field, foliar foraging by ants greatly increased when aphids were present. Higher levels of foliar foraging led to a twofold increase in the likelihood that ants contacted aphid predators. As a result of these increased encounters with ants, lacewing larvae were twice as likely to be removed from plants with aphids compared with plants without aphids. Once contact was made, however, the behaviour of ants towards lacewing larvae appeared similar between the two experimental groups.
4. Argentine ants drive away or prey upon a diversity of arthropod predators and parasitoids, but they also exhibit aggression towards certain herbivores. Future work should attempt to quantify how the ecological effects that result from interactions between honeydew-producing insects and invasive ants, such as L. humile , differ from those that result from interactions between honeydew-producing insects and native ants.     

Species-specific bird functions in a forest-canopy food web

Bird functions in a forest-canopy food web were evaluated by a large-scale field experiment using 'canopy' enclosures. By controlling the presence of two bird species, great tits (Parus major; foliage gleaner) and nuthatches (Sitta europaea; trunk gleaner), in the enclosures, their effect on predatory insects (ants), herbivorous insects (Lepidoptera larvae) and producers (oak trees) was quantified. Great tits reduced the density of Lepidoptera larvae and, indirectly, leaf damage, but had no impact on ants. Nuthatches decreased the density of ants but did not influence either Lepidoptera larvae or leaf damage. These results highlight species-specific functions of birds in the maintenance of forest ecosystems.     

Do army ant queens re-mate later in life?

Queens of eusocial Hymenoptera are inseminated only during a brief period before they start to lay eggs. This has probably been kin-selected because repeated insemination of old queens would normally be against the inclusive fitness interest of their daughter workers. Army ants have been considered to be the only possible exception to this rule due to their idiosyncratic life-history. We studied two distantly related species of army ants, the African Dorylus (Anomma) molestus and the Neotropical Eciton burchellii and present data from microsatellite genotyping, behavioural observations and sperm counts.We also describe the copulation behaviour of African army ants for the first time. Our results strongly suggest that, contradictory to earlier contentions, army ant queens do not mate repeatedly throughout their life and thus do not constitute an exception among the eusocial Hymenoptera in this respect. Sperm counts for males and queens of both species show that army ant queens have to mate with several males to become fully inseminated. However, sperm limitation by queens is unlikely to have been the prime reason for the evolution of high queen-mating frequencies in this group. Received 5 July 2006; revised 26 September 2006; accepted 11 October 2006.     

An uneasy alliance:a nesting association between aggressive ants and equally fierce social wasps

Although the Neotropical territorially dominant arboreal ant Azteca chartifex Forel is very aggressive towards any intruder,its populous colonies tolerate the close presence of the fierce polistine wasp Polybia rejecta(F.).In French Guiana,83.33%of the 48 P.rejecta nests recorded were found side by side with those of A.chartifex.This nesting association results in mutual protection from predators(i.e.,the wasps protected from army ants;the ants protected from birds).We conducted field studies,laboratorybased behavioral experiments and chemical analyses to elucidate the mechanisms allowing the persistence of this association.Due to differences in the cuticular profiles of the two species,we eliminated the possibility of chemical mimicry.Also,analyses of the carton nests did not reveal traces of marking on the envelopes.Because ant forager flows were not perturbed by extracts from the wasps’Dufour’s and venom glands,we rejected any hypothetical action of repulsive chemicals.Nevertheless,we noted that the wasps"scraped"the surface of the upper part of their nest envelope using their mandibles,likely removing the ants'scent trails,and an experiment showed that ant foragers were perturbed by the removal of their scent trails.This leads us to use the term"erasure hypothesis."Thus,this nesting association persists thanks to a relative tolerance by the ants towards wasp presence and the behavior of the wasps that allows them to"contain"their associated ants through the elimination of their scent trails,direct attacks,"wing-buzzing"behavior and ejecting the ants.     

Extraordinary Predation by the Neotropical Army Ant Cheliomyrmex andicola: Implications for the Evolution of the Army Ant Syndrome1

Workers of the genus Cheliomyrmex are unique among the New world army ants (subfamily Ecitoninae) in that their mandibles are armed with elongate, spine‐like teeth. We present the first prey records for this genus. Cheliomyrmex andicola prey on large‐bodied ground dwelling invertebrates and, possibly, on vertebrates. Unlike other army ants, C. andicola workers use their sting during prey capture. The workers' unusual mandibles and potent stings may be adapted for piercing and gripping the integument of nonarthropod prey animals, and for rapidly subduing large‐bodied prey, respectively. The genus Cheliomyrmex may be the sister taxon to other Neotropical army ants (Ecitoninae), and Cheliomyrmex shares features of mandibular morphology and prey selection with Old World driver ants in the genus Dorylus. Mass cooperative foraging, an important element of army ant behavior, may have arisen in part as an adaptation for exploiting large‐bodied prey.     

Changes in Species Richness,Abundance, and Composition of Arboreal Twig‐nesting Ants Along an Elevational Gradient in Coffee Landscapes

The distribution, diversity, and assembly of tropical insects have long intrigued ecologists, and for tropical ants, can be affected by competitive interactions, microhabitat requirements, dispersal, and availability and diversity of nesting sites. Arboreal twig‐nesting ants are limited by the number of hollow twigs available, especially in intensive agricultural systems. Ant diversity and abundance may shift along elevation gradients, but no studies have examined if the proportion of occupied twigs or richness of arboreal twig‐nesting ants vary with elevation. In coffee agroecosystems, there are over 40 species of arboreal twig‐nesting ants. We examined communities of twig‐nesting ants in coffee plants along an elevational gradient to answer the following questions: (1) Do species richness and colony abundance decline with elevation or show a mid‐elevation peak? (2) Does community composition change with elevation? (3) Is elevation an important predictor of change in ant abundance, richness, and relative abundance of common species? We surveyed 42 10 × 10 m plots in 2013 from 450 to1550 m elevation across a coffee landscape in Chiapas, Mexico. We sampled a total of 2211 hollow coffee twigs, 77.1 percent of which were occupied by one of 28 species of ants. Pseudomyrmex simplex was more abundant in lower elevations, whereas Pseudomyrmex ejectus dominated in high elevations. Species richness and the percent of occupied hollow twigs both peaked at mid‐elevations (800–1050 m). In sum, we found that species richness, abundance, and composition of arboreal twig‐nesting ants shift with elevation. These findings may provide important insights for understanding ant communities in coffee agroecosystems.     

Plant-attracted ants affect arthropod community structure but not necessarily herbivory

Abstract.  1. The effectiveness of ants as plant defenders is equivocal for plants that attract ants via extrafloral nectaries (EFNs).
2. This study focused on the myrmecophilic savannah tree Pseudocedrela kotschyi that attracts ants to EFNs and on the arthropod fauna associated with P. kotschyi . Herbivory and arthropod community composition were compared between trees that were dominated by one of three congeneric ant species, Camponotus acvapimensis , C. rufoglaucus , and C. sericeus , and between trees where ants were experimentally excluded and untreated control trees.
3. Short-term ant-exclusion experiments failed to demonstrate a consistent effect of ants on herbivory.
4. Plants dominated by different ant species differed significantly in leaf damage caused by herbivorous insects. The relative ranking of herbivory levels of the trees dominated by different ant species was persistent in three consecutive years.
5. Ants significantly reduced the abundance of different arthropod groups (Araneae, Blattodea, Coleoptera, Homoptera, non-ant Hymenoptera). Other groups, including important herbivores, seemed not to be affected (Lepidoptera, Orthoptera, Thysanoptera, Heteroptera).
6. The study suggests that the presence of ants only benefits plants when specific ant species are attracted, and protection by these ants is not counterbalanced by their negative effect on other beneficial arthropods.