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Nutrition facts of pollen: nutritional quality and how it affects reception and perception in bees
(2021)
Nutrients belong to the key elements enabling life and influencing an organism’s fitness. The intake of nutrients in the right amounts and ratios can increase fitness; strong deviations from the optimal intake target can decrease fitness. Hence, the ability to assess the nutritional profile of food would benefit animals. To achieve this, they need the according nutrient receptors, the ability to interpret the receptor information via perceptive mechanisms, and the ability to adjust their foraging behavior accordingly. Additionally, eventually existing correlations between the nutrient groups and single nutrient compounds in food could help them to achieve this adjustment. A prominent interaction between food and consumer is the interaction between flowering plants (angiosperms) and animal pollinators. Usually both of the interacting partners benefit from this mutualistic interaction. Plants are pollinated while pollinators get a (most of the times) nutritional reward in form of nectar and/or pollen. As similar interactions between plants and animals seem to have existed even before the emergence of angiosperms, these interactions between insects and angiosperms very likely have co-evolved right from their evolutionary origin. Therefore, insect pollinators with the ability to assess the nutritional profile may have shaped the nutritional profile of plant species depending on them for their reproduction via selection pressure. In Chapter I of this thesis the pollen nutritional profile of many plant species was analyzed in the context of their phylogeny and their dependence on insect pollinators. In addition, correlations between the nutrients were investigated. While the impact of phylogeny on the pollen protein content was little, the mutual outcome of both of the studies included in this chapter is that protein content of pollen is mostly influenced by the plant’s dependence on insect pollinators. Several correlations found between nutrients within and between the nutrient groups could additionally help the pollinators to assess the nutrient profile of pollen. An important prerequisite for this assessment would be that the pollinators are able to differentiate between pollen of different plant species. Therefore, in Chapter II it was investigated whether bees have this ability. Specifically, it was investigated whether honeybees are able to differentiate between pollen of two different, but closely related plant species and whether bumblebees prefer one out of three pollen mixes, when they were fed with only one of them as larvae. Honeybees indeed were able to differentiate between the pollen species and bumblebees preferred one of the pollen mixes to the pollen mix they were fed as larvae, possibly due to its nutritional content. Therefore, the basis for pollen nutrient assessment is given in bees. However, there also was a slight preference for the pollen fed as larvae compared to another non-preferred pollen mix, at least hinting at the retention of larval memory in adult bumblebees. Chapter III looks into nutrient perception of bumblebees more in detail. Here it was shown that they are principally able to perceive amino acids and differentiate between them as well as different concentrations of the same amino acid. However, they do not seem to be able to assess the amino acid content in pollen or do not focus on it, but instead seem to focus on fatty acids, for which they could not only perceive concentration differences, but also were able to differentiate between. These findings were supported by feeding experiments in which the bumblebees did not prefer any of the pollen diets containing less or more amino acids but preferred pollen with less fatty acids. In no choice feeding experiments, bumblebees receiving a diet with high fatty acid content accepted undereating other nutrients instead of overeating fat, leading to increased mortality and the inability to reproduce. Hence, the importance of fat in pollen needs to be looked into further. In conclusion, this thesis shows that the co-evolution of flowering plants and pollinating insects could be even more pronounced than thought before. Insects do not only pressure the plants to produce high quality nectar, but also pressure those plants depending on insect pollination to produce high quality pollen. The reason could be the insects’ ability to receive and perceive certain nutrients, which enables them to forage selectively leading to a higher reproductive success of plants with a pollinator-suitable nutritional pollen profile.
1. Today honey bee colonies face a wide range of challenges in modern agricultural landscapes which entails the need for a comprehensive investigation of honey bees in a landscape context and the assessment of environmental risks. Within this dissertation the pollen foraging of honey bee colonies is studied in different agricultural landscapes to gain insight into the use of pollen resources and the influence of landscape structure across the season. General suggestions for landscape management to support honey bees and other pollinators are derived.
2. Decoding of waggle dances and a subsequent spatial foraging analysis are used as methods in Chapters 4 and 5 to study honey bee colonies in agricultural landscapes. The recently developed metabarcoding of mixed pollen samples was applied for the first time in honey bee foraging ecology and allowed for a detailed analysis of pollen, that was trapped from honey bees in front hive entrances (Chapter 6).
3. Pollen identification through molecular sequencing and DNA barcoding has been proposed as an alternative approach to light microscopy, which still is a tedious and error-prone task. In this study we assessed mixed pollen probes through next-generation sequencing and developed a bioinformatic workflow to analyse these high-throughput data with a newly created reference database. To evaluate the feasibility, we compared results from classical identification based on light microscopy from the same samples with our sequencing results. Abundance estimations from sequencing data were significantly correlated with counted abundances through light microscopy. Next-generation sequencing thus presents a useful and efficient workflow to identify pollen at the genus and species level without requiring specialized palynological expert knowledge.
4. During maize flowering, four observation hives were placed in and rotated between 11 landscapes covering a gradient in maize acreage. A higher foraging frequency on maize fields compared to other landuse types showed that maize is an intensively used pollen resource for honey bee colonies. Mean foraging distances were significantly shorter for maize pollen than for other pollen origins, indicating that effort is put into collecting a diverse pollen diet. The percentage of maize pollen foragers did not increase with maize acreage in the landscape and was not reduced by grassland area as an alternative pollen resource. Our findings allow estimating the distance-related exposure risk of honey bee colonies to pollen from surrounding maize fields treated with systemic insecticides.
5. It is unknown how an increasing area of mass-flowering crops like oilseed rape (OSR) or a decrease of semi-natural habitats (SNH) change the temporal and spatial availability of pollen resources for honey bee colonies, and thus foraging distances and frequency in different habitat types. Sixteen observation hives were placed in and rotated between 16 agricultural landscapes with independent gradients of OSR and SNH area within 2 km to analyze foraging distances and frequencies. SNH and OSR reduced foraging distance at different spatial scales and depending on season, with possible benefits for the performance of honey bee colonies. Frequency of pollen foragers per habitat type was equally high for SNH, grassland and OSR fields, but lower for other crops and forest. In landscapes with a small proportion of SNH a significantly higher density of pollen foragers on SNH was observed, indicating the limitation of pollen resources in simple agricultural landscapes and the importance of SNH.
6. Quantity and diversity of collected pollen can influence the growth and health of honey bee colonies, but little is known about the influence of landscape structure on pollen diet. In a field experiment we rotated 16 honey bee colonies across 16 agricultural landscapes (see also Chapter 5), used traps to get samples of collected pollen and observed the intra-colonial dance communication to gain information about foraging distances. Neither the amount of collected pollen nor pollen diversity were related to landscape diversity. The revealed increase of foraging distances with decreasing landscape diversity suggests that honey bees compensate for a lower landscape diversity by increasing their pollen foraging range in order to maintain pollen amount and diversity.
7. Our results show the importance of diverse pollen resources for honey bee colonies in agricultural landscapes. Beside the risk of exposure to pesticides honey bees face the risk of nutritional deficiency with implications for their health. By modifying landscape composition and therefore availability of resources we are able to contribute to the wellbeing of honey bees. Agri-environmental schemes aiming to support pollinators should focus on possible spatial and temporal gaps in pollen availability and diversity in agricultural landscapes.
Entwicklung und Anwendung von Methoden zur Erfassung von Pyrrolizidinalkaloiden in Honig und Pollen
(2009)
In jüngster Vergangenheit hat die potentielle Belastung von Lebens- und Futtermitteln mit PA wiederholt Aufmerksamkeit erregt. Eine Exposition des Menschen mit PA kann über den Genuss von Tees, Phytopharmaka, pflanzlichen Lebensmitteln (z.B. Salatmischungen) oder, im Fall einer Verfütterung von PA-Pflanzen an Tiere, als sekundäre Kontamination über tierische Lebensmittel erfolgen. Im ‚International Programme on Chemical Safety (IPCS)’ der WHO ist die grundsätzliche Gefährdung der menschlichen Gesundheit durch PA dokumentiert. Aus Gründen des vorbeugenden Verbraucherschutzes gibt es demzufolge Rechtsvorschriften zur Regulierung PA-haltiger Phytopharmaka. Für diese gilt in Deutschland seit 1992 ein Grenzwert von 1 µg PA/Tag für 1,2-ungesättigte PA und deren N-Oxide bei oraler Aufnahme und einer Anwendungsdauer von max. 6 Wochen. Geht die Anwendung darüber hinaus, beträgt der Grenzwert 0,1 µg PA/Tag. Im ersten Teil der Arbeit wurde eine robuste, reproduzierbare und selektive analytische Methode basierend auf Zink-Staub-Reduktion, Festphasenextraktion (SCX-SPE), LiAlH4 Reduktion mit anschließender Silylierung sowie Kapillargaschromatographie-Massenspektrometrie (HRGC-MS)-Analytik erarbeitet. Durch ein solches Vorgehen werden die PA-N-Oxide in tertiäre PA überführt, so dass alle PA in ihrer tertiären Form vorliegen. Durch die anschließende chemische Reduktion werden alle Mono- und Diester-PA in die jeweiligen Necinbasen überführt. Durch die anschließende Derivatisierung zum di-TMS-Derivat, konnten über den Summenparameter Retronecin PA-Kontaminationen mit 1,2-ungesättigten PA-Strukturen verlässlich detektiert und hochselektiv mittels HRGC-MS im SIM-Modus angezeigt werden. Die Validierung der Methode erfolgte durch die Verwendung von Senecio vernalis-Extrakt sowie authentischen PA-Standards und deren N-Oxiden. Unter Modifikationen der Probenaufarbeitung war diese Methode sowohl für Honig und Pollen, als auch für honighaltige Lebensmittel einsetzbar. Im weiteren Verlauf der Arbeit wurde die Methode durch die Synthese des deuterierten Standards di-Butyroyl-[9,9-2H2]-Retronecin zur Stabilisotopen-Verdünnungsanalyse (SIVA) erweitert und optimiert. Die entwickelte Methode erlaubt erstmals, anders als bei bereits vorliegenden Arbeiten zur Bestimmung von PA in Pflanzenteilen, eine exakte und selektive Bestimmung von PA im Spurenbereich, unabhängig von deren botanischem Ursprung oder chemischer Struktur (tertiäres PA, N-Oxide). In einem breit aufgestellten Screening von 216 Honighandelsproben und 35 Forschungshonigen – letztere umfassten 27 Senecio- und 8 Echium-Honige - konnten zum Teil erhebliche Mengen an PA nachgewiesen werden. Die Belastungsrate der einzelnen Probensets reichte von 9 bis zu 100%. Die hierbei ermittelten Gehalte lagen, berechnet als Retronecin-Äquivalente, zwischen 0,019 µg/g und 4,66 µg/g. Ergänzt wurden die analytischen Daten durch die Erhebung von mellisopalynologischen Daten. Hierbei zeigte sich, dass eine Bestimmung von PA-Pflanzenpollen über die relative Pollenhäufigkeit nach DIN 10760 nur eine geringe Aussagekraft bei der Riskioabschätzung besitzt. Zwar war die Anwesenheit von PA-Pflanzenpollen immer ein Indikator für das Vorkommen von PA, jedoch konnten über den relativen Pollengehalt keine Aussagen über die Höhe der PA-Belastung getroffen werden. In einer weiteren Studie zu PA-Gehalten in Pollen und Pollenerzeugnissen sind in den nativen Pollen die erwartet hohen PA-Gehalte bestätigt worden. Aber auch die in Vollsortimentsupermärkten und Reformhäusern häufig vertretenen Pollenprodukte wiesen PA-Gehalte auf, die im Mittel weit über den bei Honig festgestellten Werten lagen. So ergaben sich für die nativen Pollen aller bedeutenden, PA-produzierenden Pflanzenfamilien PA-Gehalte von 0,57-4,07 mg/g, während sich für die Pollenprodukte Gehalte von 1,08-16,35 µg/g feststellen ließen. Eine zusätzliche Erhebung von mellisopalynologischen Daten bestätigte deren bereits bei den Honigproben festgestellte, eingeschränkte Aussagekraft hinsichtlich des PA-Gehaltes. Durch ein Screening von 60 honighaltigen Lebensmitteln mit unterschiedlichen Honiganteilen konnte eine potentielle Downstream-Kontamination durch den Einsatz von hoch PA-belasteten Honigen im Herstellungsprozess nachgewiesen werden. Bei einer Belastungshäufigkeit von 13% lagen die hierbei ermittelten PA-Gehalte, berechnet als Retronecin-Äquivalente, bei 0,010-0,484 µg/g. Abschließend ist in modellhaft durchgeführten Filtrationsversuchen gezeigt worden, dass PA-Pflanzenpollen erheblichen Einfluss auf den PA-Gehalt des Honigs ausüben. Dennoch stellt eine Honigfiltration, wie sie in Anlage 1 der Honigverordnung zulässig ist, keine Möglichkeit dar, hoch mit PA belasteten Honig im PA-Gehalt zu senken. Vielmehr ließ sich mit den durchgeführten Versuchen eine Diffusion der PA aus Pollen in den Honig nachweisen.
There are ample sand dune and sand sheets in the Texas Rolling Plains, U.S.A. Their varied location, morphology and paleosol content pointed to differnces in their historical develpment throughout the Holocene. Younger dunes, so called fence line dunes have been identified as remnants of unsound agricultural practices which just recently formed at the beginning of this century. Correspondingly soils were eroded, in parts, down to the C-horizon in some of these areas. More mature sand were dated with the radiocarbon method and identified having formed during the Altithermal warming period. This study identifies major eolian anthropogenic and climatic reactivation and stabilisation phases in the Rolling Plains of Texas during the Holocene, but also ties them into the existing Southern High Plains and Great Plains climatic record. This study also researched the reasons for the regional and local sand reactivation phases and contributes to the eolian history in the Great Plains region. The outline of this dissertation is oriented towards a comprehensive regional approach in cultural and physical geography. Chapter 1 covers the physiographic setting of the Rolling Plains region including geology, geomorphology, climate and vegetation. Here the prerequisites for eolian activity in the area are explained, followed by the criteria for the selection of the individual study sites. In chapter 2 selected dune fields and sand sheets are introduced. Chapter 3 outlines the methodology as a combination of field research, laboratory analysis and remote sensing techniques, along with a brief interpretation of their application and success rate. Chapter 4 investigates interactive processes between the cultural development and the physical landscape of the region. The next 4 chapters are focusing on research results and interpretation. Chapter 5 interprets the youngest eolian episodes resulting from the cultural de-velopment of the area, including a description and definition of so called "fenceline dunes" and "shinnery motts". Other dunes with very young buried horizons are also described in this chapter, and a comparison with outcrops in the Nebraska Sand Hills is performed. Chapter 6 interprets short-term, cyclic, drought related sand reactivations several hundred years ago by means of a Post Oak (Quercus stellata) tree ring record as established by STAHLE and CLEAVELAND (1988). In chapter 7 older Holocene reactivation cycles are introduced, investigating the idea of the existence of a warmer period, previously named the Altithermal, which so far has only been identified in the Southern High Plains. The last chapter (8) includes a brief statement of the study’s purpose along with the summary and discussion of results presented. This chapter will end with further implications of this research.