Wie stachellose Bienen Pflanzenharze sammeln und nutzen

Harz ist ein klebriges Pflanzenprodukt mit einem oft intensiven aromatischen Geruch. Es wird von Bäumen produziert, um Wunden zu verschließen und schädliche Besucher abzuwehren. Einige Insektenarten haben jedoch die erstaunliche Fähigkeit entwickelt, mit der klebrigen Substanz umzugehen und sie sich gar zu Nutzen zu machen. So verwenden Bienen Harz beispielsweise zum Nestbau und zur Verteidigung ihrer Kolonien. Während allgemein bekannt ist, dass Bienen Pollen und Nektar sammeln, wird der Tatsache, dass sie auch Harz sammlen, allerdings sehr viel weniger Beachtung geschenkt. Ziel meiner Dissertation war es daher, herauszufinden, warum, wie und wo stachellose Bienen in Borneo (sieben untersuchte Bienenarten), Australien (acht Arten) und Costa Rica (27 Arten) Pflanzenharze sammeln und verwerten. Diese Arbeit behandelt somit die enge Beziehung zwischen einer eusozialen Insektengattung und einem chemisch und physiologisch hoch komplexen Pflanzenprodukt, das Bienen nicht nur als Nestmaterial und zur Verteidigung dient, sondern auch eine wesentliche Bedeutung für deren chemische Diversität hat. Stachellose Bienen verhalten sich hochgradig opportunistisch, wenn sie Harz sammeln, d.h. verschiedene Bienenarten sammeln Harz von denselben Baumarten, wobei sie nahezu jede verfügbare Harzquelle nutzen. Dabei finden und erkennen sie Harzquellen anhand einiger charakteristischer Mono- und Sesquiterpene, nutzen jedoch nicht das gesamte Harz-Bouquet. Die Menge an eingetragenem Harz unterscheidet sich zwischen verschiedenen Bienenarten und kolonien und varriert mit verschiedenen Umweltbedingungen. Insbesondere eine Bedrohung durch Fressfeinde (z. B. Ameisen) führt zu einer massiven Steigerung des Harzeintrages; eine manuelle Zerstörung des Nesteinganges hat dagegen relativ wenig Einfluss. Das eingetragene Harz wird zum Nestbau und zur Verteidigung gegen Fressfeinde und Mikroben genutzt. Darüber hinaus dient es als Quelle für Terpene, die von den Bienen in ihre chemischen Oberflächenprofile eingebaut werden (kutikuläre Terpene). Dabei übertragen sie nur einen Bruchteil (8 %) der gewaltigen Menge (>> 1000) an Terpenen, die man im Harz von Bäumen findet, auf ihre Oberfläche. Die übertragenen Terpene bleiben in ihrer Struktur unverändert, allerdings unterscheiden sich die Bienenarten in der Zusammensetzung der Terpenprofile auf ihrer Oberfläche, obwohl alle untersuchten Arten Harz von denselben Bäumen sammeln. Die unterschiedlichen Terpenprofile sowie die Tatsache, dass nur wenige Terpene aus dem Harz aufgenommen werden, deuten auf einen artspezifischen und bisher unbekannten Filterungsmechanismus bei stachellosen Bienen hin. Auch übersteigt durch die Aufnahme von Terpenen die chemische Diversität der Oberflächenprofile von stachellosen Bienen die zahlreicher anderer Hymenopteren. Da Bienen die Terpene aus dem Harz nur „filtern“, sie dabei aber nicht verändern, sind sämtliche Bienenarten aus Borneo, Australien und Costa den charakteristischen Harzprofilen von Bäumen aus ihren Ursprungsgebieten chemisch sehr ähnlich. Da in jeder tropischen Region andere Baumarten vorkommen, varriert die chemische Zusammensetzung der vorkommenden Harze und damit der kutikulären Terpene von dort vorkommenden Bienen. Die meisten Bienenarten mit kutikulären Terpenen findet man in Borneo, wo nahezu 100 % der untersuchten Arten aus Baumharzen gewonnene Terpene in ihre chemischen Profilen einbauen. Im Gegensatz dazu sind es in Costa Rica nur 40 % der untersuchten Arten. Auch sammeln in Borneo gelegentlich 9 von 10 Arbeiterinnen einer Tetragonilla collina Kolonie Harz, wohingegen in Australien maximal 10 % und in Costa Rica maximal 40 % der Arbeiterinnen einer Kolonie Harz sammeln. Das Vorherrschen von Harz und aus Harz gewonnenen Terpenen in der chemischen Ökologie von Bienen auf Borneo spiegelt das Vorherrschen einer bestimmten südostasiatischen Baumfamilie wieder: der Dipterocarpaceen, deren Holz ungewöhnlich harzig ist. Ein solch enger Zusammenhang zwischen der Chemie von Bienen und der von Baumharzen verdeutlicht die enge Beziehung zwischen stachellosen Bienen und den Bäumen in ihrem Habitat. Die kutikulären Terpene schützen ihre Träger vor Angreifern (z.B. Ameisen) und Mikrobenbefall. Dabei variiert eine bestimmte Gruppe – Sesquiterpene – am meisten zwischen den Arten. Diese Terpengruppe manipuliert die natürlichweise auftretende zwischen-artliche Aggression, indem sie letztere bei jenen Arten verringert, die selbst keine Sesquiterpene in ihrem Profil haben. Aggressionsminderung durch chemische Komponenten, welche aus der Umwelt aufgenommen werden, stellt somit einen bisher unbekannten Mechanismus dar, um Toleranz zwischen sonst aggressiven Arten zu erreichen. Eine derarte Herabsetzung von aggressiven Verhalten bei stachellosen Bienen kann darüber hinaus ein entscheidender Faktor für das Entstehen sogenannter Nestaggregationen sein. Dabei nisten Kolonien von Bienenarten mit und Bienenarten ohne Sesquiterpene in ihrem chemischen Profil in unmittelbarer Nachbarschaft, ohne gegeneinander aggressiv zu sein. Im Hinblick auf die zahlreichen Funktionen, die Harze und/oder aus dem Harz gewonnene Substanzen für stachellose Bienen haben, stellt Harz zweifelsohne eine bedeutende Ressource in der Welt der Bienen dar – eine Ressource, die einen direkten Einfluss auf deren chemische Ökologie, Verteidigungsmechanismen und zwischen-artliche Kommunikation ausübt. Wie genau die Bienen ihre artspezifischen Terpenprofile erzeugen, insbesondere, wie es ihnen gelingt, dabei ganze Terpengruppen auszuschließen, muss in zukünftigen Studien genauer untersucht werden. Auch stellt sich die Frage, wie wichtig eine hohe Diversität an Harzquellen und damit Baumarten für die Bienen ist! Es ist durchaus möglich, dass neben einer Vielfalt an Blütenpflanzenarten auch der „Harzreichtum“ für das Wohlergehen der Bienen eine entscheidende Rolle spielt.Resin, a sticky sap emitting terpenoids and other volatiles, is produced by various plant species to seal wounds and protect themselves against herbivores and microbes. Among several other insects, bees have evolved the surprising ability to handle the repellent plant sap and use it to construct and defend their nests. Whereas the collection of pollen and nectar has been intensively studied in bees, resin collection has received only little attention. The aim of this dissertation was to better understand how the physiological and chemical properties of resin and resin-derived compounds (terpenes) affect the ecology of stingless bees. I therefore asked why, where and how stingless bees of Borneo (seven study-species), Australia (eight) and Costa Rica (27) collect and process plant resins, addressing the importance of a largely neglected resource not only for building and defensive properties, but also for the bees’ chemical diversity. Stingless bees are highly opportunistic resin foragers with all species collecting resin from a similar set of tree species. They locate and/or recognize resin sources on the basis of several volatile mono- and sesquiterpenes. I found that different bee species and even colonies significantly varied in the amount of resin collected. Predator attack (e.g., by ants) had the strongest affect on resin intake, whereas manual nest destruction only slightly increased the number of resin foragers. Resin is used to build, maintain and defend nests, but also as source for chemical compounds (terpenes) which stingless bees include in their surface profiles (chemical profiles). They directly transfer resin-derived compounds to their body surfaces (cuticular terpenes), but only include a subset (8 %) of the large number (>> 1000) of terpenes found in tree resins. This phenomenon can only be explained by a hitherto unknown ability to filter environmentally derived compounds which results in species-specific terpene profiles and thus in an increased chemical heterogeneity among species. Moreover, due to the addition of resin-derived substances the diversity of compounds on the bees’ body surfaces by far exceeds the chemical diversity of profiles in other hymenopterans. Because stingless bees filter but do not modify resin-derived compounds, species from Borneo, Australia and Costa Rica all resemble the characteristic resin of typical trees in their regions of origin. This chemical similarity reveals a strong correlation between the diversity of tree resins and the diversity of cuticular terpenes among stingless bees in a given habitat. Because different tree species are found in different tropical regions, the chemical composition of tree resins varies between tropical regions as does the composition of cuticular terpenes in bee species from these regions. Cuticular terpenes are however most common among stingless from Borneo, with 100 % of species studied having resin-derived terpenes in their chemical profiles. They are least common in Costa Rica, with only 40 % of species having terpenes. Likewise, resin collection was found to be highest in Tetragonilla collina colonies of Borneo where occasionally up to 90 % of foragers collected resin. By contrast, resin collection was only performed by 10 % of foragers of a given colony in Australia and by a maximum of 40 % in Costa Rica. The dominance of resin and resin-derived compounds in the chemical ecology of bees from Borneo may mirror the dominance of a particular Southeast Asian tree family: the highly resinous dipterocarps. Such a correlation between the chemistry of bees and the chemistry of tree resins therefore underlines the close relationship between stingless bees and the trees of their habitat. Cuticular terpenes are assumed to protect bees against predators and/or microbes. Sesquiterpenes, a specific group of terpenes, most vary between species and impair inter-specific aggression by reducing aggressive behavior in species without sesquiterpenes, thereby providing a novel mechanism to achieve interspecific tolerance among insects. Reduced interspecific aggression may also be an important factor enabling the non-aggressive aggregation of nests from stingless bee colonies of up to four different species, because such aggregations frequently comprise both species with and species without sesquiterpenes. Given its various functions, resin represents a highly important resource for stingless bees which directly affects their chemical ecology, defensive properties and inter-specific communication. It remains to be investigated how the bees influence the resin-derived terpene profiles on their body surface and in their nests, particularly how they manage to exclude entire groups of terpenes. Whether bees actually need a high diversity of different resin sources and therefore tree species to maintain the homeostasis of their colonies or whether they would do equally well with a limited amount of resin sources available, should also be addressed in future studies. Answers to this question will directly impair bee and forest management in (sub)tropical regions

The same, but different: pollen foraging in honeybee and bumblebee colonies

Like many other bees worldwide, honeybees and bumblebees are threatened by human-induced disturbances. Yet some species decline and others thrive, likely due to different foraging strategies. As little is known about how resource intake translates into nutrients available to colonies, our study aimed to better understand how differences in foraging strategies may affect colony health by relating differences in pollen spectra collected to differences in nutrient composition. The Apis and Bombus colonies studied were all located at the same site, but nevertheless differed in the spectra of plant species visited for pollen collection and the quality of pollen collected. Bumblebees generally collected pollen with significantly higher pollen protein content and more essential amino acids. Unlike honeybees that tend to exploit large resource patches, bumblebees thus seem to select the “better” pollen and to focus on quality instead of quantity

Do Hybrid Trees Inherit Invasive Characteristics? Fruits of Corymbia torelliana X C. citriodora Hybrids and Potential for Seed Dispersal by Bees

Tree invasions have substantial impacts on biodiversity and ecosystem functioning, and trees that are dispersed by animals are more likely to become invasive. In addition, hybridisation between plants is well documented as a source of new weeds, as hybrids gain new characteristics that allow them to become invasive. Corymbia torelliana is an invasive tree with an unusual animal dispersal mechanism: seed dispersal by stingless bees, that hybridizes readily with other species. We examined hybrids between C. torelliana and C. citriodora subsp. citriodora to determine whether hybrids have inherited the seed dispersal characteristics of C. torelliana that allow bee dispersal. Some hybrid fruits displayed the characteristic hollowness, resin production and resin chemistry associated with seed dispersal by bees. However, we did not observe bees foraging on any hybrid fruits until they had been damaged. We conclude that C. torelliana and C. citriodora subsp. citriodora hybrids can inherit some fruit characters that are associated with dispersal by bees, but we did not find a hybrid with the complete set of characters that would enable bee dispersal. However, around 20,000 hybrids have been planted in Australia, and ongoing monitoring is necessary to identify any hybrids that may become invasive

Smelling like resin: terpenoids account for species-specific cuticular profiles in Southeast-Asian stingless bees

Insects may be unique in having a cuticle with a species-specific chemical profile. In social insects, colony survival depends not only on species-specific but also on colony-specific cuticular compounds with hydrocarbons playing an important role in the communication systems of ants, termites, wasps and bees. We investigated inter- and intraspecific differences in the composition of compounds found on the body surface of seven paleotropical stingless bee species (Apidae: Meliponini) at two different sites in Borneo (Sabah, Malaysia). Besides hydrocarbons, the body surface of all seven stingless bee species comprised terpenoid compounds, a substance class that has not been reported for chemical profiles of any social insect so far. Moreover, the chemical profile of some species differed fundamentally in the composition of terpenoids with one group (e.g. sesquiterpenes) being present in one species, but missing in another. Chemical profiles of different colonies from the same species showed the same hydrocarbon- and terpenoid compounds over different regions, as tested for Tetragonilla collina and Tetragonula melanocephala. However, chemical profiles differed quantitatively between the different colonies especially in T. melanocephala. It is likely that the terpenoids are derived from plant resins because stingless bees are known to collect and use large amounts of resins for nest construction and defence, suggesting an environmental origin of the terpenoids in the chemical profile of paleotropical stingless bees

Diets maintained in a changing world: Does land-use intensification alter wild bee communities by selecting for flexible generalists?

Biodiversity loss, as often found in intensively managed agricultural landscapes, correlates with reduced ecosystem functioning, for example, pollination by insects, and with altered plant composition, diversity, and abundance. But how does this change in floral resource diversity and composition relate to occurrence and resource use patterns of trap-nesting solitary bees? To better understand the impact of land-use intensification on communities of trap-nesting solitary bees in managed grasslands, we investigated their pollen foraging, reproductive fitness, and the nutritional quality of larval food along a land-use intensity gradient in Germany. We found bee species diversity to decrease with increasing land-use intensity irrespective of region-specific community compositions and interaction networks. Land use also strongly affected the diversity and composition of pollen collected by bees. Lack of suitable pollen sources likely explains the absence of several bee species at sites of high land-use intensity. The only species present throughout, Osmia bicornis (red mason bee), foraged on largely different pollen sources across sites. In doing so, it maintained a relatively stable, albeit variable nutritional quality of larval diets (i.e., protein to lipid (P:L) ratio). The observed changes in bee–plant pollen interaction patterns indicate that only the flexible generalists, such as O. bicornis, may be able to compensate the strong alterations in floral resource landscapes and to obtain food of sufficient quality through readily shifting to alternative plant sources. In contrast, other, less flexible, bee species disappear

The role of non-volatile chemicals of floral rewards in plant-pollinator interactions

The interaction between plants and pollinators has intrigued scientists for centuries. While it continues to be [a] subject of ongoing research in basic and applied ecology, we tend to ignore that plant-pollinator interactions are largely driven by chemistry. For example, the amounts and composition of various chemical compounds determine flower colour, the attractiveness of scent and the nutritional value of floral rewards. In this perspective article, we focus on the chemistry of pollen and nectar. We discuss differences in the function, diversity and variation of compound groups that are considered macro- and micronutrients for pollinators as well as in non-nutritive plant secondary metabolites (PSM). We highlight that effects of and pollinator responses to different compounds vary strongly among pollinator species and (groups of) compounds. Moreover, we challenge the commonly applied separation between toxic (e.g. several PSMs) and beneficial (e.g. most nutrients) compounds and point to a dose-dependent toxicity across compounds. We finally provide a list of open questions for future research. We draw particular attention to the unknown effects that interactions between plant-produced compounds and externally applied compounds (e.g. pesticides, pollutants) may have on the plant-pollinator mutualism

Foraging loads of stingless bees and utilisation of stored nectar for pollen harvesting

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Stingless bees use terpenes as olfactory cues to find resin sources

Insects largely rely on olfactory cues when seeking and judging information on nests, partners, or resources. Bees are known to use volatile compounds - besides visual cues - to find flowers suitable for pollen and nectar collection. Tropical stingless bees additionally collect large amounts of plant resins for nest construction, nest maintenance, nest defense, and to derive chemical constituents for their cuticular profiles. We here demonstrate that stingless bees of Borneo also use olfactory cues to find tree resins. They rely on volatile mono- and sesquiterpenes to locate or recognize known resin sources. Moreover, by modifying resin extracts, we found that stingless bees do not use the entire resin bouquet but relative proportions of several terpenes. In doing so, the bees are able to learn specific tree resin profiles and distinguish between tree species and partly even tree individuals