Ulrich Maschwitz

Diversity of ant-plant interactions : protective efficacy in Macaranga species with different degrees of ant association

The pioneer tree Macaranga in SE Asia has developed manyfold associations with ants. The genus comprises all stages of interaction with ants, from facultative relationships to obligate myrmecophytes. Only myrmecophytic Macaranga offer nesting space for ants and are associated with a specific ant partner. The nonmyrmecophytic species are visited by a variety of different ant species which are attracted by extrafloral nectaries (EFN) and food bodies. Transitional Macaranga species like M. hosei are colonized later in their development due to their stem structure. Before the colonization by their specific Crematogaster partner the young plants are visited by different ant species attracted by EFN. These nectaries are reduced and food body production starts as soon as colonization becomes possible. We demonstrated earlier that obligate ant partners can protect their Macaranga plants against herbivore damage and vine cover. In this study we focused on nonspecific interactions and studied M. tanarius and M. hosei, representing a non-myrmecophyte and a transitional species respectively. In ant exclusion experiments both M. tanarius and M. hosei suffered significantly higher mean leaf damage than controls, 37% versus 6% in M. hosei, 16% versus 7% in M. tanarius. M. tanarius offers both EFN and food bodies so that tests for different effects of these two food rewards could be conducted. Plants with food bodies removed but with EFN remaining had the lowest mean increase of herbivore damage of all experimental groups. Main herbivores on M. hosei were mites and caterpillars. Many M. tanarius plants were infested by a shootborer. Both Macaranga species were visited by various ant species, Crematogaster spp. being the most abundant. We found no evidence for any specific relationships. The results of this study strongly support the hypothesis that non-specific, facultative associations with ants can be advantageous for Macaranga plants. Food bodies appear to have lower attractive value for opportunistic ants than EFN and may require a specific dietary adaptation. This is also indicated by the fact that food body production in the transitional M. hosei does not start before stem structure allows a colonization by the obligate Crematogaster species. M. hosei thus benefits from facultative association with a variety of ants until it produces its first domatia and can be colonized by its obligate mutualist.

Slippery ant-plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae)

Abstract In many ant-plant species of the genus Macaranga in South-East Asia, conspicuous blooms of epicuticular wax crystals cover the stem surface. We found that many ant species were unable to walk on these surfaces. Only the specific ant partners of glaucous Macaranga host plants were capable of moving on the slippery stems without difficulty. Therefore, the epicuticular coatings of Macaranga myrmecophytes appear to have a selective function and protect the associated ants against competitors. The epicuticular aggregates function as a physical barrier; no evidence of chemical repellence was found. The extent to which ”foreign” ant species are excluded from a tree strongly depends on inclination, diameter and length of the glaucous stem sections. The particular growth form of some glaucous Macaranga ant-plants enhances the influence of the wax barriers. The ant associates of glaucous and glossy Macaranga ant-plants (genera Crematogaster and Camponotus) differ strongly in their capacity to adhere to the glaucous stems. For this reason, the wax blooms in Macaranga can act as an ecological isolation mechanism for the sympiotic ants. Within the genus Macaranga, we find a high correspondence between the occurrence of glaucousness and obligatory ant association (50% in ant-plants; 6.7% in non-myrmecophytes). The genus Macaranga thus represents one of the few cases known so far where epicuticular wax crystals are likely to have evolved in relation to insects.

Studies on the south east Asian ant-plant associationCrematogaster borneensis/Macaranga: Adaptations of the ant partner

SummaryC. borneensis (Myrmicinae) lives in close association with several myrmecophytic species of the South East Asian pioneer tree genusMacaranga (Euphorbiaceae). The ants are adapted to the plants so closely that they do not survive away from it. The only food they utilize is provided as food bodies by the plant and honeydew from specific scale insects kept inside the hollow internodes. The anatomy of the digestive tract is also adapted to life on the host plant: the crop is very small and can store only minute food quantities. C. borneensis exclusively colonizes certainMacaranga species. Queens as well as workers are able to recognize their host plant species, probably by chemical cues. Colony founding queens swarm throughout the year, mostly during darkness. There is strong competition among queens for host plants. Queens do not carry scale insects on their nuptial flight. Worker ants are active day and night. Most of them patrol and collect food bodies on the younger parts of the host plant. An important characteristic is their cleaning behaviour, which results in removal of all foreign objects. Even though they are rather small, workers respond very aggressively to certain kinds of disturbance of the host plant. The ants attack most phytophagous insects and are especially effective in killing and removing small, softbodied herbivores (e.g. caterpillars). They do not possess a functional sting, but apply defensive secretion and—once biting an intruder—will not let go. Their effective alarm system results in a mass attack, which provides adequate defence for the colony and the host plant. A comparison with anotherCrematogaster species further illustrated the special adaptations ofC. borneensis to its host plant.ZusammenfassungC. borneensis (Myrmicinae) lebt in enger Gemeinschaft mit myrmekophytischen Arten der südostasiatischen PionierbaumgattungMacaranga (Euphorbiaceae). Die Ameise ist so eng an die Pflanze adaptiert, daß sie getrennt von ihr nicht lebensfähig ist. Die Nahrung beziehtC. borneensis in Form von Nährkörperchen ausschließlich von der Pflanze. Im Sproßachseninnern gehaltene spezifische Schildläuse bieten eine weitere Nahrungsquelle. Die Adaptationen erstrecken sich bis auf die Anatomie des Verdauungstraktes: Der Kropf ist sehr klein und kann nur geringe Nahrungsmengen speichern. C. borneensis besiedelt spezifisch nurMacaranga-Pflanzen. Sowohl Königinnen als auch Arbeiterinnen sind in der Lage, die Wirtspflanze zu erkennen, wobei offenbar chemische Reize eine Rolle spielen. Die koloniegründenden Königinnen schwärmen das gesamte Jahr über, das Schwärmen erfolgt überwiegend während der Dunkelheit. Um die besiedlungsfähigenMacaranga-Pflanzen herrscht ein starker Konkurrenzdruck. Die beteiligten Schildlausarten sind spezifisch für die Assoziation. Sie werden nicht von der Königin beim Hochzeitsflug mitgenommen. Die Arbeiterinnen sind tag- und nachtaktiv. Die meisten Tiere halten sich im jüngsten Drittel der Pflanze auf, wo sie patrouillieren und Nährkörperchen sammeln. Mittels eines spezifischen Säuberungsverhaltens entfernen die Arbeiterinnen alle Fremdobjekte von der Pflanze.Trotz ihrer geringen Größe attackieren die Ameisen eine Vielzahl phytophager Insekten und sind dabei besonders effektiv in der Abwehr kleiner, wenig sklerotisierter Tiere wie z.B. Raupen. Sie verfügen zwar nicht über einen funktionsfähigen Stachel, setzen aber wehrsekrete ein und beißen sich hartnäckig fest. Mit Hilfe eines effektiven Alarmierungssystems, das einen Massenangriff ermöglicht, gewährleisten sie eine Verteidigung ihrer Kolonien und damit gleichzeitig ihrer Wirtspflanze. Eine Vergleich mit einer anderenCrematogaster-Art demonstriert die besonderen Adaptationen vonC. borneensis an ihre Wirtspflanze.

Communication by tandem running in the antCamponotus sericeus

Summary1.Camponotus sericeus recruits nestmates to newly discovered food sources or nest sites by the tandem running technique.2.The food alarm consists of short lasting fast runs inside the nest and brief food offerings. The “invitation behavior” for following to new nest sites is different: a recruiter faces a nestmate, grips it on the mandibles, pulls it forward and while turning around 180 °, loosens the grasp and presents the gaster. When the leader is then touched at the gaster or hindlegs by the follower, tandem running starts.3.Dummy experiments have shown that these tactile stimuli are important to release leadership behavior during tandem running. Furthermore we demonstrated that the follower ant is bound to the leader by a surface pheromone. In addition a mechanical contact to the leader ensures a precise orientation during tandem following.4.The leader ant discharges a trail pheromone out of the hindgut. It has been shown that these chemical trails are not important for recruitment in the tandem running technique. However, they are used as orientation cues.Zusammenfassung1.Camponotus sericeus wirbt Neulinge zu Futter- und Nestplätzen durch Tandemlauf. Nachdem eine Nestgenossin durch ein spezifisches Aufforderungsverhalten stimuliert wurde, folgt sie dicht hinter der Führerin.2.Das Aufforderungsverhalten bei der Werbung zu Futterplätzen und Nestplätzen ist verschieden: Im ersten Fall werden die Nestgenossinnen durch Erregungsläufe und kurzes Futteranbieten stimuliert, im letzteren Fall wird die Ameise kurz an den Mandibeln gezogen, bevor sich die werbende Ameise umdreht und der Nestgenossin die Gaster bietet. Der Tandemlauf beginnt, wenn die geworbene Ameise mit Antennen und Kopf gegen Gaster und Hinterbeine der Führerin trommelt.3.Attrappenversuche haben gezeigt, daß diese taktilen Signale entscheidend für das Auslösen des Führverhaltens sind. Weiterhin wurde nachgewiesen, daß die Folgeameise durch chemische Signale (Oberflächenpheromone) an die Führerin gebunden ist. Zusätzliche mechanische Signale erleichtern die Orientierung beim Folgen.4.Die Führameise gibt aus dem Enddarm eine Spursubstanz ab, die jedoch keine Bedeutung für den Tandemlauf oder für das Werbeverhalten hat. Sie dient offensichtlich nur als Orientierungsspur.

Vergleichende Untersuchungen zur Funktion der Ameisenmetathorakaldrüse

SummaryIn 6 of 7 ant subfamilies investigated, the workers produce an acidic secretion in their metapleural glands. With the exception of the gland fluid of Cremastogaster (Physocrema) inflata, all tested secretions were found to suppress the growth of Escherichia coli. From this and from former results, it is concluded that the metapleural gland contents function as an antiseptic.In Cremastogaster inflata the metapleural gland is greatly enlarged. The workers release the highly sticky secretion when attacked and so immobilize their arthropod enemies. In addition the fluid releases alarm behavior; the antiseptic gland has become a defence-alarm gland.The acidic antibiotic secretion from the enlarged metapleural glands of Cremastogaster (Physocrema) difformis is not sticky. It is constantly discharging in small quantities protecting the colony against microorganisms. When workers fight against animal enemies, the discharge can be increased. Enemies are repelled by the irritating tar-like smell.ZusammenfassungBei 6 von 7 untersuchten Ameisenunterfamilien erzeugen die Arbeiterinnen ein säurehaltiges Metathorakaldrüsensekret (+: Myrmicinae, Ponerinae, Pseudomyrmicinae, Myrmeciinae, Aneuretinae, Dolichoderinae;-: Dorylinae). Mit Ausnahme des Sekrets von Cremastogaster inflata hemmen die getesteten Drüsenflüssigkeiten das Wachstum von Escherichia coli. Hieraus und aus früheren Befunden wird auf eine Antiseptikafunktion der Metathorakaldrüse geschlossen.Bei Cremastogaster (Physocrema) inflata sind die Metathorakaldrüsen extrem vergrößert. Die Arbeiterinnen geben das stark klebrige Sekret bei Gefahr aktiv ab und immobilisieren damit ihre Arthropodenfeinde. Zusätzlich löst das Sekret Gefahrenalarm aus. Die Antiseptikadrüse ist zu einer Wehr-Alarmdrüse geworden.Das saure, antibiotisch wirksame Sekret aus der hypertrophierten Drüse von Cremastogaster (Physocrema) difformis ist nicht klebrig. Es tritt ständig in kleinen Mengen aus und schützt damit das Volk gegen Mikroorganismen. Beim Kampf der Arbeiterinnen mit tierischen Gegnern kann es vermehrt frei werden und diese durch seinen stark teerartigen Geruch vertreiben.In 6 of 7 ant subfamilies investigated, the workers produce an acidic secretion in their metapleural glands. With the exception of the gland fluid of Cremastogaster (Physocrema) inflata, all tested secretions were found to suppress the growth of Escherichia coli. From this and from former results, it is concluded that the metapleural gland contents function as an antiseptic.In Cremastogaster inflata the metapleural gland is greatly enlarged. The workers release the highly sticky secretion when attacked and so immobilize their arthropod enemies. In addition the fluid releases alarm behavior; the antiseptic gland has become a defence-alarm gland.The acidic antibiotic secretion from the enlarged metapleural glands of Cremastogaster (Physocrema) difformis is not sticky. It is constantly discharging in small quantities protecting the colony against microorganisms. When workers fight against animal enemies, the discharge can be increased. Enemies are repelled by the irritating tar-like smell.

Foraging strategies and recruitment behaviour in the European harvester ant Messor rufitarsis (F.)

SummaryMost of the approximately 40 species of the Old World harvester ant genus Messor live in warm and dry Mediterranean areas. One species, M. rufitarsis, is found in isolated Northern temperate habitats in Rheinhessen and the Rheingau area in Hessen, West Germany. These habitats are characterized by a great diversity of spermatophytes, so that permanently changing seed resources are available for the ants during the growing period. M. rufitarsis has maintained its granivorous specialization under these habitat conditions and collects most of the seed resources, which show a large fluctuation in quantity, quality and distributional pattern throughout the year. M. rufitarsis is very flexible in using different foraging strategies. For discovering newly ripened food resources and collecting wide-spread single seeds, an individual foraging strategy is used. However, dense seed resources are exploited through an effective recruitment system. Nestmates are guided to the feeding place by means of orientation-recruitment trails from Dufours gland. Additional invitation behaviour enhances the success of recruitment. From analysis of slow-motion movies it is concluded that stridulation is the crucial signal of the invitation behaviour.

The migrating herdsman Dolichoderus (Diabolus) cuspidatus: an ant with a novel mode of life

SummaryThe Malayan ant Dolichoderus cuspidatus lives in obligatory symbiosis with the pseudococcid Malaicoccus formicarii and other species of the same genus. The assemblies, which may be encountered up to 25 m away from the nest, are constantly covered with a great number of worker ants who protect them and receive honeydew. In the event of heavy rain the workers from a dense protective cluster, clinging to each other on top of the mealybugs. Neither hunting behavior nor active search for protein sources was observed in D. cuspidatus, although dead insects were accepted as food. When not searching for new plants, the activity of the ants outside the colony is limited to visiting the mealybugs. During the night and parts of the day the ants stay in their nest. Ant colonies deprived of their mealybugs are not viable due to their dependence on the symbiosis and because of the competition of other ants. Antless M. formicarii are likewise not viable. The mealybugs are extremely polyphagous and feed on many different monocotylous and dicotylous angiosperms. They feed exclusively on the phloem sap of young plant parts which are rich in amino acids. Dolichoderus cuspidatus workers carry the mealybugs to such locations. During the picking up and carrying process both partners display typical behavioral patterns. The colonization of new feeding sites takes place in well organized mass processions. During the foundation or disintegration of large feeding complexes, provisional depots with waiting mealybugs and ants are set up. The pseudococcids are carried not only while shifting the feeding sites, but also whenever the colony leaves its former nesting site and especially when any kind of disturbance occurs. They are even carried about without any apparent external cause, which leads to the fact that, at all times of trail activity, on average more than 10% of all ants using the trails carry mealybugs. Mealybugs are also present within the nest, especially adult females which are viviparous and give birth to their offspring there. Censused colonies each consisted of over 10 000 workers, about 4000 larvae and pupae, more than 5000 mealybugs and one ergatoid queen. Male winged ants were observed in large numbers during the dry season (January–February) and during the rainy season (September–October). The colonies form typical clumplike bivouac nests consisting of clusters of workers clinging to each other, thereby covering the brood and the mealybugs. The nesting site is in no way altered by constructive measures and is mostly found close to the ground. The preferred nesting sites are clusters of leaves, and cavities in wood or soil, although a freely hanging bivouac between a few branches may be set up as well. As soon as the distance between the nest and the feeding site is too great the colony moves to the feeding site, whereby the brood and the mealybugs are carried along in a well organized manner. During such nest-moving the establishment of intermediate depots can be observed. A shift of nest sites can also be induced by disturbances or by a change in the microclimate in the vicinity of the nest. Colonies multiply by budding. The tropical rain forest continuously offers different sprouting plants, the utilization of which requires extreme mobility on the part of the consumer. The unique behavioral strategy of D. cuspidatus, to carry constantly their polyphagous mealybug partners to new feeding sites and to take the whole colony there has enabled this ant and its symbiont to occupy this rich food niche. Dolichoderus cuspidatus is the first true nomad found in ants.

Der Hochzeitsschwarm der Rossameise Camponotus herculeanus L. (Hym. formicidae)

Zusammenfassung1.Im Untersuchungsgebiet (Gramschatzer Wald bei Würzburg/Ufr.) schwärmt Camponotus herculeanus von Mitte Mai bis Mitte Juni. Jedes Nest mit jungen Geschlechtstieren bringt zwei bis fünf Hauptschwärme hervor.2.Camponotus herculeanus zeigt eine ausgeprägte Schwarmvorbereitung, in der dem späteren Schwärmen ein charakteristisches „Sonnungsverhalten“ beider Geschlechter vorausgeht.3.Die Temperatur steuert wesentlich Intensität und Zeitpunkt des Schwärmens; primär unterliegen aber „Sonnung“, Schwarmbeginn und Schwarmablauf einem tagesrhythmischen Verlauf. Der Schwarmflug findet zwischen 17 und 19 Uhr statt.4.Das Schwärmen beginnt mit dem Auszug der Männchen; der Weibchenabflug setzt schlagartig im Abflugsmaximum der Männchen ein. Die Männchen starten in Fluglochhöhe, die Weibchen klettern am Nestbaum bis zu den Astspitzen empor und schwärmen von dort ab.5.Das Zusammenfallen der Abflugmaxima beider Geschlechter wird durch ein Duftsignal gesteuert. Die Männchen geben in Fluglochnähe in höchster Schwarmerregung das stark riechende Sekret der Mandibeldrüse ab, das die Weibchen zum Auslaufen und zum Abflug veranlaßt. Die Stimulationswirkung des Mandibeldrüsensekrets der Männchen ist umso vollkommener, je näher der natürliche Schwarmzeitpunkt — bezogen sowohl auf Jahres- als auch auf Tageszeit — rückt.6.Der Duft der Männchen wirkt nur stimulierend auf die Weibchen, nicht anlockend.7.Der Mandibeldrüsenduft der Männchen von Camponotus ligniperda wirkt auf Weibchen von C. herculeanus ebenfalls stimulierend.8.Die biologische Bedeutung des koordinierten Abschwärmens der Geschlechter wird diskutiert.Summary1.In the area of Würzburg (Westgermany) Camponotus herculeanus swarms from mid-may till the middle of June. Each nest containing young sexually mature ants produces from 2 up to 5 swarms.2.A characteristic “sun bathing” of both sexes precedes the mating flight.3.Intensity and timing of swarming depend on temperature. Sun bathing behavior as well as onset and performance of swarming show a diurnal rhythmicity. The mating flight starts between 5 and 7 PM.4.The males begin swarming, the females swarm starts like an avalanche just when the bulk of the males takes off at the level of the flight hole. The females climb the branches of the tree and then fligh off.5.The swarming of the bulk of both sexes is synchronized by odor. The males release during highest swarming activity a strongly smelling secretion from their mandibular glands which stimulates the females to take off, too. The alarming efficiency of the secretion increases the closer the natural time for the take off approaches — both in regard to season and daytime.6.The females are only stimulated to take off by the odor not attracted.7.Females of Camponotus herculeanus are not only stimulated by the mandibular secretion of the males of their own species but also by that of males of C. ligniperda.8.The biological significance of the coordinated mass flight is discussed.

Thrips pollination of the dioecious ant plant Macaranga hullettii (Euphorbiaceae) in Southeast Asia

Discussion about thrips (Thysanoptera) as main pollinators has been controversial in the past because thrips do not fit the preconception of an effective pollinator. In this study, we present evidence for thrips pollination in the dioecious pioneer tree genus Macaranga (Euphorbiaceae). Macaranga hullettii is pollinated predominantly by one thrips species, Neoheegeria sp. (Phlaeothripidae, Thysanoptera). As a reward for pollinators, the protective floral bracteoles function as breeding sites for thrips and trichomal nectaries on the adaxial surface of the floral bracteoles provide alimentation. Flowering phenology of both staminate and pistillate trees was highly synchronized within 3-4 wk periods. In contrast to pistillate trees, staminate trees start to breed the thrips inside the developing inflorescences ∼2 wk before anthesis. Breeding of Neoheegeria sp. in the laboratory indicates that the thrips development is completed within ∼17 d. Thus, staminate trees offer breeding sites for one thrips generation until the onset of pollen presentation. Intraspecific pollen transfer by thrips was proved by pollen loads of thrips taken from receptive pistillate inflorescences of M. hullettii. Bagging experiments of different mesh sizes showed that seed set reached almost the level of open-pollinated flowers when exclusively tiny insects like thrips were able to enter the net bags, but no apomictic seed set occurred when no insect access was given to the flowers.

The soft scale (Coccidae) associates of Malaysian ant-plants

Myrmecophytic species of the Paleotropical plant genus Macaranga (Euphorbiaceae) have hollow stems that are almost always occupied by ants of the genus Crematogaster and scale insects of the family Coccidae (Hemiptera: Coccoidea). The coccids have a cryptic endophytic lifestyle and are confined to this microhabitat. They are much more diverse than previously recognised. First data are presented on the diversity, prevalence, specificity and distribution of the coccids associated with myrmecophytic Macaranga species. Twenty-two species of Coccidae in total, including 15 previously unknown from Macaranga, were disco- vered from 19 species of Macaranga in Peninsular Malaysia and Borneo. The ori- ginal describers tentatively assigned the known coccid species to Coccus (Coccinae) but the Macaranga coccids still require taxonomic research to establish their correct placing. The coccids varied in their host-plant specificity from species that occurred in most of the sampled Macaranga to one species that was found almost exclusively only on a single host species. In addition to their occurrence on Macar- anga, only three species, C. macarangae and C. secretus and morphospecies C. 214 were found on rare occasions in the stem interior of a few other myrmecophytes and in a non-myrmecophytic liana, but did not regularly colonise these plants. Most of the coccids can be regarded as highly specific at the plant genus level.