Publications by authors named "Karl Crailsheim"

40 Publications

Prisoners receive food fit for a queen: honeybees feed small hive beetles protein-rich glandular secretions through trophallaxis.

J Exp Biol 2021 01 27;224(Pt 2). Epub 2021 Jan 27.

Social Insects Research Group, Department of Zoology and Entomology, University of Pretoria, Private Bag X20, Hatfield 0028, South Africa.

The honeybee nest parasite (small hive beetle) uses behavioural mimicry to induce trophallactic feeding from its honeybee hosts. Small hive beetles are able to induce honeybee workers to share the carbohydrate-rich contents of their crops, but it is not clear whether the beetles are able to induce to workers to feed them the protein-rich hypopharyngeal glandular secretions fed to the queen, larvae and other nest mates. Protein is a limiting macronutrient in an insect's diet, essential for survival, growth and fecundity. Honeybees obtain protein from pollen, which is consumed and digested by nurse bees. They then distribute the protein to the rest of the colony in the form of hypopharyngeal gland secretions. Using C-phenylalanine as a qualitative marker for protein transfer, we show that small hive beetles successfully induce worker bees to feed them the protein-rich secretions of their hypopharyngeal glands during trophallaxis, and that females are more successful than males in inducing the transfer of these protein-rich secretions. Furthermore, behavioural observations demonstrated that female beetles do not preferentially interact with a specific age cohort of bees when soliciting food, but males tend to be more discriminant and avoid the more aggressive and active older bees.
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http://dx.doi.org/10.1242/jeb.234807DOI Listing
January 2021

A citizen science supported study on seasonal diversity and monoflorality of pollen collected by honey bees in Austria.

Sci Rep 2019 11 12;9(1):16633. Epub 2019 Nov 12.

University of Graz, Institute of Biology, Universitätsplatz 2, 8010, Graz, Austria.

Austrian beekeepers participated in the "C.S.I. Pollen" study as citizen scientists and collected pollen from honey bee colonies in hive mounted traps every three weeks from April to September in 2014 and 2015 to uncover the seasonal availability of pollen sources for bees. 1622 pollen samples were collected and analysed using palynological light microscopy to the lowest taxonomic level possible. For 2014 and 2015 combined, 239 pollen types from more than 85 families were detected. 'Various unknown' species, Taraxacum-form and Plantago spp. were the pollen types collected by the majority of colonies (occurrence), whereas the most pollen grains collected were from Trifolium repens-form, Plantago spp. and Salix spp. (abundance). In spring, trees were found to be the most abundant pollen source, whereas in summer herbs dominated. On average, a colony collected pollen from 16.8 ± 4.7 (2014) and 15.0 ± 4.4 (2015) pollen types per sampling. Those numbers, however, vary between sampling dates and indicate a seasonal pattern. This is also supported by Simpson's diversity index, which was on median 0.668. In both years, 50.0% of analysed pollen samples were partially (>50%) and 4.2% were highly monofloral (i.e. containing >90% of one pollen type). Prevalence of monofloral pollen samples peaked at the beginning and the end of the season, when pollen diversity was the lowest.
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http://dx.doi.org/10.1038/s41598-019-53016-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6851371PMC
November 2019

Health status of honey bee colonies (Apis mellifera) and disease-related risk factors for colony losses in Austria.

PLoS One 2019 9;14(7):e0219293. Epub 2019 Jul 9.

Department for Apiculture and Bee Protection, Institute for Seed and Propagating Material, Phytosanitary Service and Apiculture, Division for Food Security, Austrian Agency for Health and Food Safety Ltd., Vienna, Vienna, Austria.

Austrian beekeepers frequently suffered severe colony losses during the last decade similar to trends all over Europe. This first surveillance study aimed to describe the health status of Austrian bee colonies and to analyze the reasons for losses for both the summer and winter season in Austria. In this study 189 apiaries all over Austria were selected using a stratified random sampling approach and inspected three times between July 2015 and spring 2016 by trained bee inspectors. The inspectors made interviews with the beekeepers about their beekeeping practice and the history of the involved colonies. They inspected a total of 1596 colonies for symptoms of nine bee pests and diseases (four of them notifiable diseases) and took bee samples for varroa mite infestation analysis. The most frequently detected diseases were three brood diseases: Varroosis, Chalkbrood and Sacbrood. The notifiable bee pests Aethina tumida and Tropilaelaps spp. were not detected. During the study period 10.8% of the 1596 observed colonies died. Winter proved to be the most critical season, in which 75% of the reported colony losses happened. Risks for suffering summer losses increased significantly, when colonies were weak in July, had queen problems or a high varroa mite infestation level on bees in July. Risks for suffering winter losses increased significantly, when the colonies had a high varroa mite infestation level on bees in September, were weak in September, had a queen older than one year or the beekeeper had few years of beekeeping experience. However, the effect of a high varroa mite infestation level in September had by far the greatest potential to raise the winter losses compared to the other significant factors.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0219293PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6615611PMC
February 2020

Investigating the role of landscape composition on honey bee colony winter mortality: A long-term analysis.

Sci Rep 2018 08 16;8(1):12263. Epub 2018 Aug 16.

University of Graz, Institute of Biology, Graz, 8010, Austria.

The health of honey bee colonies is, amongst others, affected by the amount, quality and diversity of available melliferous plants. Since landscape is highly diverse throughout Austria regarding the availability of nutritional resources, we used data from annual surveys on honey bee colony losses ranging over six years to analyse a possible relationship with land use. The data set comprises reports from a total of 6,655 beekeepers and 129,428 wintered honey bee colonies. Regions surrounding the beekeeping operations were assigned to one of six clusters according to their composition of land use categories by use of a hierarchical cluster analysis, allowing a rough distinction between urban regions, regions predominated by semi-natural areas and pastures, and mainly agricultural environments. We ran a Generalised Linear Mixed Model and found winter colony mortality significantly affected by operation size, year, and cluster membership, but also by the interaction of year and cluster membership. Honey bee colonies in regions composed predominantly of semi-natural areas, coniferous forests and pastures had the lowest loss probability in four out of six years, and loss probabilities within these regions were significantly lower in five out of six years compared to those within regions composed predominantly of artificial surfaces, broad-leaved and coniferous forest.
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http://dx.doi.org/10.1038/s41598-018-30891-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6095838PMC
August 2018

Does the Pollen Diet Influence the Production and Expression of Antimicrobial Peptides in Individual Honey Bees?

Insects 2018 Jul 4;9(3). Epub 2018 Jul 4.

Institute of Biology, University of Graz, Universitätsplatz 2, 8010 Graz, Austria.

We investigated the importance of protein nutrition for honey bee immunity. Different protein diets (monofloral pollen of spp., spp., spp., spp., a mixture of the four different pollen and the pollen substitute Feedbee) were fed to honey bees in cages . After 18 days of feeding, apidaecin 1 isoforms concentration in the thorax were measured using nanoflow liquid chromatography coupled with mass spectrometry. Expression levels of genes, coding for apidaecins and abaecin in the abdomen were determined using quantitative PCR. The results indicate that protein-containing nutrition in adult worker honey bees can trigger certain metabolic responses. Bees without dietary protein showed lower apidaecin 1 isoforms concentrations. The significantly lowest concentration of apidaecin 1 isoforms was found in the group that was fed no pollen diet when compared to , , , and pollen or the pollen supplement FeedBee. Expression levels of the respective genes were also affected by the protein diets and different expression levels of these two antimicrobial peptides were found. Positive correlation between concentration and gene expression of apidaecins was found. The significance of feeding bees with different protein diets, as well as the importance of pollen nutrition for honey bee immunity is demonstrated.
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http://dx.doi.org/10.3390/insects9030079DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6164669PMC
July 2018

Protein nutrition governs within-host race of honey bee pathogens.

Sci Rep 2017 11 8;7(1):14988. Epub 2017 Nov 8.

Institute of Bee Health, Vetsuisse Faculty, University of Bern, Bern, Switzerland.

Multiple infections are common in honey bees, Apis mellifera, but the possible role of nutrition in this regard is poorly understood. Microsporidian infections, which are promoted by protein-fed, can negatively correlate with virus infections, but the role of protein nutrition for the microsporidian-virus interface is unknown. Here, we challenged naturally deformed wing virus - B (DWV-B) infected adult honey bee workers fed with or without pollen ( = protein) in hoarding cages, with the microsporidian Nosema ceranae. Bee mortality was recorded for 14 days and N. ceranae spore loads and DWV-B titers were quantified. Amongst the groups inoculated with N. ceranae, more spores were counted in protein-fed bees. However, N. ceranae infected bees without protein-diet had reduced longevity compared to all other groups. N. ceranae infection had no effect on protein-fed bee's longevity, whereas bees supplied only with sugar-water showed reduced survival. Our data also support that protein-feeding can have a significant negative impact on virus infections in insects. The negative correlation between N. ceranae spore loads and DWV-B titers was stronger expressed in protein-fed hosts. Proteins not only enhance survival of infected hosts, but also significantly shape the microsporidian-virus interface, probably due to increased spore production and enhanced host immunity.
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http://dx.doi.org/10.1038/s41598-017-15358-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5678143PMC
November 2017

Food consumption and food exchange of caged honey bees using a radioactive labelled sugar solution.

PLoS One 2017 29;12(3):e0174684. Epub 2017 Mar 29.

Institute of Zoology, University of Graz, Graz, Austria.

We measured the distribution of sugar solution within groups of caged honey bees (Apis mellifera) under standard in vitro laboratory conditions using 14C polyethylene glycol as a radioactive marker to analyze ingestion by individual bees after group feeding. We studied the impact of different experimental setups by varying the number of bees, age of bees, origin of bees, duration of experiment, the amount of available diet, and the influence of the neurotoxic pesticide imidacloprid in the diet on the feeding and food sharing behavior (trophallaxis). Sugar solution was non-uniformly distributed in bees in 36 out of 135 cages. As a measure of the extent to which the sugar diet was equally distributed between caged bees, we calculated the (inner 80%) intake ratio by dividing the intake of the 90th percentile bee by the intake of the 10th percentile bee. This intake ratio ranged from 1.3 to 94.8 in 133 individual cages, further supporting a non-uniform distribution of food among caged bees. We can expect a cage with 10 or 30 bees containing one bee that ingests, on average, the 8.8-fold of the bee in the same cage ingesting the smallest quantity of food. Inner 80% intake ratios were lower in experiments with a permanent or chronic offering of labelled sugar solution compared to temporary or acute feedings. After pooling the data of replicates to achieve a higher statistical power we compared different experimental setups. We found that uniform food distribution is best approached with 10 newly emerged bees per cage, which originate from a brood comb from a single colony. We also investigated the trophallaxis between caged honey bees which originally consumed the diet and newly added bees. Color marked bees were starved and added to the cages in a ratio of 10:5 or 20:20 after the initial set of bees consumed all the labelled sugar solution. The distribution of the labelled sugar solution by trophallaxis within 48 hours to added bees was 25% (10:5) or 45% (20:20) of the initial sugar solution. Imidacloprid at its median lethal dose (LD50) in the sugar solution reduced this post-feeding food transmission to 27% (20:20). Our results show that differences in food intake exist within caged bees that may lead to differential exposure that can influence the interpretation of toxicity tests.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0174684PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5371368PMC
September 2017

Cuticular hydrocarbon cues of immune-challenged workers elicit immune activation in honeybee queens.

Mol Ecol 2017 Jun 1;26(11):3062-3073. Epub 2017 Apr 1.

Department of Zoology, Karl-Franzens University of Graz, Universitätsplatz 2, A-8010, Graz, Austria.

Recently, evidence has shown that variations in the cuticular hydrocarbons (CHCs) profile allow healthy honeybees to identify diseased nestmates, eliciting agonistic responses in the former. Here, we determined whether these 'immunologic cues' emitted by diseased nestmates were only detected by workers, who consequently took hygienic measures and excluded these individuals from the colony, or whether queens were also able to detect these cues and respond accordingly. Healthy honeybee queens were exposed to (i) healthy, (ii) Ringer-injected and (iii) lipopolysaccharide (LPS)-injected nestmates by allowing direct body contact. Quantitative differences in the CHC profiles of these three groups were measured using GC-MS. The transcript levels of the products of four genes that encode for antimicrobial peptides (AMPs), which are part of the queen's immune response, were measured in bees exposed to direct contact using qPCR. A significant increase in the transcript levels of these AMP genes over baseline levels in queens was observed when body contact was allowed between the queens and the Ringer- and LPS-injected nestmates. These results provide the first evidence that the detection of CHCs contributes to the initiation of an immune response in insects. In an additional experiment, CHCs were extracted from diseased workers and directly presented to queens, which also evoked a similar immune response. A potential mechanism that relied on volatile compounds could be ruled out by conducting a distance experiment. The study helps to expand our knowledge of chemical communication in insects and sheds light on a likely new mechanism of social immunity.
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http://dx.doi.org/10.1111/mec.14086DOI Listing
June 2017

Sublethal pesticide doses negatively affect survival and the cellular responses in American foulbrood-infected honeybee larvae.

Sci Rep 2017 02 1;7:40853. Epub 2017 Feb 1.

Institute of Zoology, Universitätsplatz 2, University of Graz, A-8010 Graz, Austria.

Disclosing interactions between pesticides and bee infections is of most interest to understand challenges that pollinators are facing and to which extent bee health is compromised. Here, we address the individual and combined effect that three different pesticides (dimethoate, clothianidin and fluvalinate) and an American foulbrood (AFB) infection have on mortality and the cellular immune response of honeybee larvae. We demonstrate for the first time a synergistic interaction when larvae are exposed to sublethal doses of dimethoate or clothianidin in combination with Paenibacillus larvae, the causative agent of AFB. A significantly higher mortality than the expected sum of the effects of each individual stressor was observed in co-exposed larvae, which was in parallel with a drastic reduction of the total and differential hemocyte counts. Our results underline that characterizing the cellular response of larvae to individual and combined stressors allows unmasking previously undetected sublethal effects of pesticides in colony health.
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http://dx.doi.org/10.1038/srep40853DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5286422PMC
February 2017

Modelling seasonal effects of temperature and precipitation on honey bee winter mortality in a temperate climate.

Sci Total Environ 2017 Feb 2;579:1581-1587. Epub 2016 Dec 2.

University of Graz, Institute of Zoology, Universitätsplatz 2, 8010 Graz, Austria.

Insect pollinators are essential to global food production. For this reason, it is alarming that honey bee (Apis mellifera) populations across the world have recently seen increased rates of mortality. These changes in colony mortality are often ascribed to one or more factors including parasites, diseases, pesticides, nutrition, habitat dynamics, weather and/or climate. However, the effect of climate on colony mortality has never been demonstrated. Therefore, in this study, we focus on longer-term weather conditions and/or climate's influence on honey bee winter mortality rates across Austria. Statistical correlations between monthly climate variables and winter mortality rates were investigated. Our results indicate that warmer and drier weather conditions in the preceding year were accompanied by increased winter mortality. We subsequently built a statistical model to predict colony mortality using temperature and precipitation data as predictors. Our model reduces the mean absolute error between predicted and observed colony mortalities by 9% and is statistically significant at the 99.9% confidence level. This is the first study to show clear evidence of a link between climate variability and honey bee winter mortality.
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http://dx.doi.org/10.1016/j.scitotenv.2016.11.178DOI Listing
February 2017

How a life-like system emerges from a simple particle motion law.

Sci Rep 2016 11 30;6:37969. Epub 2016 Nov 30.

Department for Zoology, Karl-Franzens University Graz, Austria.

Self-structuring patterns can be observed all over the universe, from galaxies to molecules to living matter, yet their emergence is waiting for full understanding. We discovered a simple motion law for moving and interacting self-propelled particles leading to a self-structuring, self-reproducing and self-sustaining life-like system. The patterns emerging within this system resemble patterns found in living organisms. The emergent cells we found show a distinct life cycle and even create their own ecosystem from scratch. These structures grow and reproduce on their own, show self-driven behavior and interact with each other. Here we analyze the macroscopic properties of the emerging ecology, as well as the microscopic properties of the mechanism that leads to it. Basic properties of the emerging structures (size distributions, longevity) are analyzed as well as their resilience against sensor or actuation noise. Finally, we explore parameter space for potential other candidates of life. The generality and simplicity of the motion law provokes the thought that one fundamental rule, described by one simple equation yields various structures in nature: it may work on different time- and size scales, ranging from the self-structuring universe, to emergence of living beings, down to the emergent subatomic formation of matter.
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http://dx.doi.org/10.1038/srep37969DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5346932PMC
November 2016

Lysophosphatidylcholine acts in the constitutive immune defence against American foulbrood in adult honeybees.

Sci Rep 2016 08 2;6:30699. Epub 2016 Aug 2.

Institute of Zoology, Universitätsplatz 2, University of Graz, 8010 Graz, Austria.

Honeybee (Apis mellifera) imagines are resistant to the Gram-positive bacterium Paenibacillus larvae (P. larvae), causative agent of American foulbrood (AFB), whereas honeybee larvae show susceptibility against this pathogen only during the first 48 h of their life. It is known that midgut homogenate of adult honeybees as well as a homogenate of aged larvae exhibit strong anti-P. larvae activity. A bioactivity-guided LC-HRMS analysis of midgut homogenate resulted in the identification of 1-oleoyl-sn-glycero-3-phosphocholine (LPC) pointing to a yet unknown immune defence in adult honeybees against P. larvae. Antimicrobial activity of LPC was also demonstrated against Melissococcus plutonius, causative agent of European Foulbrood. To demonstrate an AFB-preventive effect of LPC in larvae, artificially reared larvae were supplemented with LPC to evaluate its toxicity and to assess whether, after infection with P. larvae spores, LPC supplementation prevents AFB infection. 10 μg LPC per larva applied for 3 d significantly lowered mortality due to AFB in comparison to controls. A potential delivery route of LPC to the larvae in a colony via nurse bees was assessed through a tracking experiment using fluorescent-labelled LPC. This yet undescribed and non-proteinous defense of honeybees against P. larvae may offer new perspectives for a treatment of AFB without the utilization of classic antibiotics.
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http://dx.doi.org/10.1038/srep30699DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4969740PMC
August 2016

Hit-and-run trophallaxis of small hive beetles.

Ecol Evol 2015 12 6;5(23):5478-86. Epub 2015 Nov 6.

Social Insect research Group Department of Zoology and Entomology University of Pretoria 0002 Pretoria South Africa.

Some parasites of social insects are able to exploit the exchange of food between nestmates via trophallaxis, because they are chemically disguised as nestmates. However, a few parasites succeed in trophallactic solicitation although they are attacked by workers. The underlying mechanisms are not well understood. The small hive beetle (=SHB), Aethina tumida, is such a parasite of honey bee, Apis mellifera, colonies and is able to induce trophallaxis. Here, we investigate whether SHB trophallactic solicitation is innate and affected by sex and experience. We quantified characteristics of the trophallactic solicitation in SHBs from laboratory-reared individuals that were either bee-naïve or had 5 days experience. The data clearly show that SHB trophallactic solicitation is innate and further suggest that it can be influenced by both experience and sex. Inexperienced SHB males begged more often than any of the other groups had longer breaks than their experienced counterparts and a longer soliciting duration than both experienced SHB males and females, suggesting that they start rather slowly and gain more from experience. Successful experienced females and males were not significantly different from each other in relation to successful trophallactic interactions, but had a significantly shorter soliciting duration compared to all other groups, except successful inexperienced females. Trophallactic solicitation success, feeding duration and begging duration were not significantly affected by either SHB sex or experience, supporting the notion that these behaviors are important for survival in host colonies. Overall, success seems to be governed by quality rather than quantity of interactions, thereby probably limiting both SHB energy investment and chance of injury (<1%). Trophallactic solicitation by SHBs is a singular example for an alternative strategy to exploit insect societies without requiring chemical disguise. Hit-and-run trophallaxis is an attractive test system to get an insight into trophallaxis in the social insects.
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http://dx.doi.org/10.1002/ece3.1806DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4813108PMC
December 2015

Effect of hydroxymethylfurfural (HMF) on mortality of artificially reared honey bee larvae (Apis mellifera carnica).

Ecotoxicology 2016 Mar 21;25(2):320-8. Epub 2015 Nov 21.

Institute of Zoology, Karl-Franzens University of Graz, Universitätsplatz 2, 8010, Graz, Austria.

Hydroxymethylfurfural (HMF) is a heat-formed, acid-catalyzed contaminant of sugar syrups, which find their way into honey bee feeding. As HMF was noted to be toxic to adult honey bees, we investigated the toxicity of HMF towards larvae. Therefore we exposed artificially reared larvae to a chronic HMF intoxication over 6 days using 6 different concentrations (5, 50, 750, 5000, 7500 and 10,000 ppm) and a control. The mortality was assessed from day 2 to day 7 (d7) and on day 22 (d22). Concentrations ranging from 5 to 750 ppm HMF did not show any influence on larval or pupal mortality compared to controls (p > 0.05; Kaplan-Meier analysis). Concentrations of 7500 ppm or higher caused a larval mortality of 100%. An experimental LC50 of 4280 ppm (d7) and 2424 ppm (d22) was determined. The calculated LD50 was 778 µg HMF per larva on d7 and 441 µg HMF on d22. Additionally, we exposed adult honey bees to high concentrations of HMF to compare the mortality to the results from larvae. On d7 larvae are much more sensitive against HMF than adult honey bees after 6 days of feeding. However, on d22 after emergence adults show a lower LC50, which indicates a higher sensitivity than larvae. As toxicity of HMF against honey bees is a function of time and concentration, our results indicate that HMF in supplemental food will probably not cause great brood losses. Yet sublethal effects might decrease fitness of the colony.
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http://dx.doi.org/10.1007/s10646-015-1590-xDOI Listing
March 2016

Early maternal loss affects social integration of chimpanzees throughout their lifetime.

Sci Rep 2015 Nov 10;5:16439. Epub 2015 Nov 10.

Department of Cognitive Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.

The long-term effects of early adverse experiences on later psychosocial functioning are well described in humans, but sparsely documented for chimpanzees. In our earlier studies, we investigated the effects of maternal and social deprivation on three groups of ex-laboratory chimpanzees who experienced either an early or later onset of long-term deprivation. Here we expand our research by adding data on subjects that came from two stable zoo groups. The groups comprised of early maternally deprived wild-caught chimpanzees and non-deprived zoo-born chimpanzees. We found that compared to zoo chimpanzees, ex-laboratory chimpanzees were more restricted regarding their association partners in the newly formed groups, but not during their second year of group-life, indicating that social stability has an important influence on the toleration of association partners close-by. Social grooming activity, however, was impaired in early long-term deprived ex-laboratory chimpanzees as well as in early maternally deprived zoo chimpanzees compared to non-deprived zoo chimpanzees. Thus, we conclude that early maternal loss has lifelong effects on the social integration of chimpanzees which becomes evident in their grooming networks. Although the retrospective nature of our study prevents a clear causal explanation, our results are of importance for understanding the development of social competence in chimpanzees.
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http://dx.doi.org/10.1038/srep16439DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4639738PMC
November 2015

From honeybees to robots and back: division of labour based on partitioning social inhibition.

Bioinspir Biomim 2015 Oct 26;10(6):066005. Epub 2015 Oct 26.

Artificial Life Lab of the Department of Zoology, Universitätsplatz 2, Karl-Franzens University Graz, A-8010 Graz, Austria.

In this paper, a distributed adaptive partitioning algorithm inspired by division of labor in honeybees is investigated for its applicability in a swarm of underwater robots in one hand and is qualitatively compared with the behavior of honeybee colonies on the other hand. The algorithm, partitioning social inhibition (PSI), is based on local interactions and uses a simple logic inspired from age-polyethism and task allocation in honeybee colonies. The algorithm is analyzed in simulation and is successfully applied here to partition a swarm of underwater robots into groups demonstrating its adaptivity to changes and applicability in real world systems. In a turn towards the inspiration origins of the algorithm, three honeybee colonies are then studied for age-polyethism behaviors and the results are contrasted with a simulated swarm running the PSI algorithm. Similar effects are detected in both the biological and simulated swarms suggesting biological plausibility of the mechanisms employed by the artificial system.
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http://dx.doi.org/10.1088/1748-3190/10/6/066005DOI Listing
October 2015

Immune responses of honeybees and their fitness costs as compared to bumblebees.

Apidologie 2015;46(2):238-249. Epub 2014 Oct 17.

Department of Zoology, Universitätsplatz 2, Karl-Franzens University of Graz, A-8010 Graz, Austria.

Immune responses of invertebrates imply more than developing a merely unspecific response to an infection. Great interest has been raised to unveil whether this investment into immunity also involves fitness costs associated to the individual or the group. Focusing on the immune responses of honeybees, we use the well-studied insect bumblebee for comparison. Bumblebees are capable of producing specific immune responses to infections whereas this has not been assessed for honeybees so far. We investigated whether a prior bacterial encounter provides protection against a later exposure to the same or a different bacterium in honeybees. Additionally, we studied whether the foraging activities of honeybees and bumblebees are affected upon immune stimulation by assessing the flight performance. Finally, the acceptance behavior of nestmates toward immune-challenged honeybees was determined. Results show that despite stimulating the immune system of honeybees, no protective effects to infections were found. Further, honeybees were not affected by an immune challenge in their flight performance whereas bumblebees showed significant flight impairment. Immune-challenged honeybees showed lower survival rates than naive individuals when introduced into a regular colony. Here, we reveal different immune response-cost scenarios in honeybees and bumblebees for the first time.
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http://dx.doi.org/10.1007/s13592-014-0318-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4579911PMC
October 2014

In vitro growth inhibition by Hypericum extracts and isolated pure compounds of Paenibacillus larvae, a lethal disease affecting honeybees worldwide.

Chem Biodivers 2014 May;11(5):695-708

Institute of Zoology, Karl-Franzens-University Graz, Universitätsplatz 2, A-8010 Graz.

The in vitro inhibitory potential of 50 extracts from various species of the flowering plant genus Hypericum was investigated using the Kirby-Bauer disk diffusion susceptibility test against Paenibacillus larvae, a spore-forming, Gram-positive bacterial pathogen that causes American foulbrood (AFB), a lethal disease affecting honeybee brood worldwide. Of the tested extracts, 14 were identified as highly active against P. larvae as compared to the activity of the positive control, indicating the presence of highly potent antibacterial compounds in the extracts. Examination of these extracts using TLC and HPLC/MS analyses revealed the presence of acylphloroglucinol and filicinic-acid derivatives. Six pure compounds isolated from these extracts, viz., hyperforin (1), uliginosin B (2), uliginosin A (3), 7-epiclusianone (4), albaspidin AA (5), and drummondin E (6), displayed strong antibacterial activity against the vegetative form of P. larvae (MIC ranging from 0.168-220 μM). Incubation of P. larvae spores with the lipophilic extract of Hypericum perforatum and its main acylphloroglucinol constituent 1 led to the observation of significantly fewer colony forming units as compared to the negative control, indicating that the acylphloroglucinol scaffold represents an interesting lead structure for the development of new AFB control agents.
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http://dx.doi.org/10.1002/cbdv.201300399DOI Listing
May 2014

Trans-generational immune priming in honeybees.

Proc Biol Sci 2014 Jun 30;281(1785):20140454. Epub 2014 Apr 30.

Department of Zoology, Karl-Franzens University of Graz, , Universitätsplatz 2, 8010 Graz, Austria.

Maternal immune experience acquired during pathogen exposure and passed on to progeny to enhance resistance to infection is called trans-generational immune priming (TgIP). In eusocial insects like honeybees, TgIP would result in a significant improvement of health at individual and colony level. Demonstrated in invertebrates other than honeybees, TgIP has not yet been fully elucidated in terms of intensity and molecular mechanisms underlying this response. Here, we immune-stimulated honeybee queens with Paenibacillus larvae (Pl), a spore-forming bacterium causing American Foulbrood, the most deadly bee brood disease worldwide. Subsequently, offspring of stimulated queens were exposed to spores of Pl and mortality rates were measured to evaluate maternal transfer of immunity. Our data substantiate the existence of TgIP effects in honeybees by direct evaluation of offspring resistance to bacterial infection. A further aspect of this study was to investigate a potential correlation between immune priming responses and prohaemocytes-haemocyte differentiation processes in larvae. The results point out that a priming effect triggers differentiation of prohaemocytes to haemocytes. However, the mechanisms underlying TgIP responses are still elusive and require future investigation.
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http://dx.doi.org/10.1098/rspb.2014.0454DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4024302PMC
June 2014

Development of a new method to track multiple honey bees with complex behaviors on a flat laboratory arena.

PLoS One 2014 20;9(1):e84656. Epub 2014 Jan 20.

School of Human Science and Environment, University of Hyogo, Himeji, Hyogo, Japan.

A computer program that tracks animal behavior, thereby revealing various features and mechanisms of social animals, is a powerful tool in ethological research. Because honeybee colonies are populated by thousands of bees, individuals co-exist in high physical densities and are difficult to track unless specifically tagged, which can affect behavior. In addition, honeybees react to light and recordings must be made under special red-light conditions, which the eyes of bees perceive as darkness. The resulting video images are scarcely distinguishable. We have developed a new algorithm, K-Track, for tracking numerous bees in a flat laboratory arena. Our program implements three main processes: (A) The object (bee's) region is detected by simple threshold processing on gray scale images, (B) Individuals are identified by size, shape and spatiotemporal positional changes, and (C) Centers of mass of identified individuals are connected through all movie frames to yield individual behavioral trajectories. The tracking performance of our software was evaluated on movies of mobile multi-artificial agents and of 16 bees walking around a circular arena. K-Track accurately traced the trajectories of both artificial agents and bees. In the latter case, K-track outperformed Ctrax, well-known software for tracking multiple animals. To investigate interaction events in detail, we manually identified five interaction categories; 'crossing', 'touching', 'passing', 'overlapping' and 'waiting', and examined the extent to which the models accurately identified these categories from bee's interactions. All 7 identified failures occurred near a wall at the outer edge of the arena. Finally, K-Track and Ctrax successfully tracked 77 and 60 of 84 recorded interactive events, respectively. K-Track identified multiple bees on a flat surface and tracked their speed changes and encounters with other bees, with good performance.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0084656PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3896341PMC
December 2014

Sensitization to Hymenoptera venoms is common, but systemic sting reactions are rare.

J Allergy Clin Immunol 2014 Jun 22;133(6):1635-43.e1. Epub 2013 Dec 22.

Department of Dermatology, Division of Environmental Dermatology and Venerology, Medical University of Graz, Graz, Austria.

Background: Sensitization to Hymenoptera venom without systemic sting reactions (SSRs) is commonly observed in the general population. Clinical relevance for a future sting has not yet been investigated.

Objective: We aimed to evaluate the effect of these debatable sensitizations with deliberate sting challenges and to monitor serologic changes for up to 2 years.

Methods: One hundred thirty-one challenges with bees and wasps were performed in 94 subjects with a hitherto irrelevant sensitization. The clinical outcome was recorded, and results of specific IgE (sIgE) determinations, skin tests, and basophil activation tests were correlated to the sting reaction. sIgE levels were monitored in reactors and nonreactors after 3 hours, 1 week, 4 weeks, and 1 year.

Results: Only 5 (5.3%) patients had SSRs, but 41 (43.6%) had large local reactions (LLRs) after the sting. Compared with the general population, there was a 9.5-fold higher risk for LLRs but not for SSRs. Three hours after the sting, sIgE levels slightly decreased, but none of the 94 subjects' results turned negative. After 1 week, sIgE levels already increased, increasing up to 3.5-fold (range, 0.2- to 34.0-fold) baseline levels after 4 weeks. To assess the clinical relevance of this increase, we randomly selected 18 patients for a re-sting. Again, 50% had an LLR, but none had an SSR.

Conclusion: Although sensitization to Hymenoptera venoms was common, the risk of SSRs in sensitized subjects was low in our study. The sIgE level increase after the sting was not an indicator for conversion into symptomatic sensitization. Currently available tests were not able to distinguish between asymptomatic sensitization, LLRs, and SSRs.
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http://dx.doi.org/10.1016/j.jaci.2013.10.046DOI Listing
June 2014

Dynamics of collective decision making of honeybees in complex temperature fields.

PLoS One 2013 16;8(10):e76250. Epub 2013 Oct 16.

Artificial Life Laboratory of the Department of Zoology, Karl-Franzens University Graz, Graz, Austria.

Endothermic heat production is a crucial evolutionary adaptation that is, amongst others, responsible for the great success of honeybees. Endothermy ensures the survival of the colonies in harsh environments and is involved in the maintenance of the brood nest temperature, which is fundamental for the breeding and further development of healthy individuals and thus the foraging and reproduction success of this species. Freshly emerged honeybees are not yet able to produce heat endothermically and thus developed behavioural patterns that result in the location of these young bees within the warm brood nest where they further develop and perform tasks for the colony. Previous studies showed that groups of young ectothermic honeybees exposed to a temperature gradient collectively aggregate at the optimal place with their preferred temperature of 36 °C but most single bees do not locate themselves at the optimum. In this work we further investigate the behavioural patterns that lead to this collective thermotaxis. We tested single and groups of young bees concerning their ability to discriminate a local from a global temperature optimum and, for groups of bees, analysed the speed of the decision making process as well as density dependent effects by varying group sizes. We found that the majority of tested single bees do not locate themselves at the optimum whereas sufficiently large groups of bees are able to collectively discriminate a suboptimal temperature spot and aggregate at 36 °C. Larger groups decide faster than smaller ones, but in larger groups a higher percentage of bees may switch to the sub-optimum due to crowding effects. We show that the collective thermotaxis is a simple but well evolved, scalable and robust social behaviour that enables the collective of bees to perform complex tasks despite the limited abilities of each individual.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0076250PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3797801PMC
August 2014

Algorithmic requirements for swarm intelligence in differently coupled collective systems.

Chaos Solitons Fractals 2013 May;50(100):100-114

Artificial Life Laboratory at the Department of Zoology, Karl-Franzens University Graz, Universitätsplatz 2, A-8010 Graz, Austria.

Swarm systems are based on intermediate connectivity between individuals and dynamic neighborhoods. In natural swarms self-organizing principles bring their agents to that favorable level of connectivity. They serve as interesting sources of inspiration for control algorithms in swarm robotics on the one hand, and in modular robotics on the other hand. In this paper we demonstrate and compare a set of bio-inspired algorithms that are used to control the collective behavior of swarms and modular systems: BEECLUST, AHHS (hormone controllers), FGRN (fractal genetic regulatory networks), and VE (virtual embryogenesis). We demonstrate how such bio-inspired control paradigms bring their host systems to a level of intermediate connectivity, what delivers sufficient robustness to these systems for collective decentralized control. In parallel, these algorithms allow sufficient volatility of shared information within these systems to help preventing local optima and deadlock situations, this way keeping those systems flexible and adaptive in dynamic non-deterministic environments.
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http://dx.doi.org/10.1016/j.chaos.2013.01.011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3688318PMC
May 2013

Long-Term Evaluation of Abnormal Behavior in Adult Ex-laboratory Chimpanzees (Pan troglodytes) Following Re-socialization.

Behav Sci (Basel) 2013 Mar 31;3(1):99-119. Epub 2013 Jan 31.

Institute of Zoology, Karl-Franzens-University of Graz, Universitaetsplatz 2, 8010 Graz, Austria; E-Mails: (C.F.-S.); (K.C.).

Adverse rearing conditions are considered a major factor in the development of abnormal behavior. We investigated the overall levels, the prevalence and the diversity of abnormal behavior of 18 adult former laboratory chimpanzees, who spent about 20 years single caged, over a two-year period following re-socialization. According to the onset of deprivation, the individuals were classified as early deprived (EDs, mean: 1.2 years) or late deprived (LDs, mean: 3.6 years). The results are based on 187.5 hours of scan sampling distributed over three sample periods: subsequent to re-socialization and during the first and second year of group-living. While the overall levels and the diversity of abnormal behavior remained stable over time in this study population, the amplifying effects of age at onset of deprivation became apparent as the overall levels of abnormal behavior of EDs were far above those of LDs in the first and second year of group-living, but not immediately after re-socialization. The most prevalent abnormal behaviors, including eating disorders and self-directed behaviors, however, varied in their occurrence within subjects across the periods. Most important, the significance of social companionship became obvious as the most severe forms of abnormal behavior, such as dissociative and self-injurious behaviors declined.
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http://dx.doi.org/10.3390/bs3010099DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4217617PMC
March 2013

Analysis of swarm behaviors based on an inversion of the fluctuation theorem.

Artif Life 2014 1;20(1):77-93. Epub 2013 Feb 1.

Karl-Franzens University Graz, University of Paderborn.

A grand challenge in the field of artificial life is to find a general theory of emergent self-organizing systems. In swarm systems most of the observed complexity is based on motion of simple entities. Similarly, statistical mechanics focuses on collective properties induced by the motion of many interacting particles. In this article we apply methods from statistical mechanics to swarm systems. We try to explain the emergent behavior of a simulated swarm by applying methods based on the fluctuation theorem. Empirical results indicate that swarms are able to produce negative entropy within an isolated subsystem due to frozen accidents. Individuals of a swarm are able to locally detect fluctuations of the global entropy measure and store them, if they are negative entropy productions. By accumulating these stored fluctuations over time the swarm as a whole is producing negative entropy and the system ends up in an ordered state. We claim that this indicates the existence of an inverted fluctuation theorem for emergent self-organizing dissipative systems. This approach bears the potential of general applicability.
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http://dx.doi.org/10.1162/ARTL_a_00097DOI Listing
March 2014

A hormone-based controller for evaluation-minimal evolution in decentrally controlled systems.

Artif Life 2012 22;18(2):165-98. Epub 2012 Feb 22.

Karl-Franzens University Graz, Austria.

One of the main challenges in automatic controller synthesis is to develop methods that can successfully be applied for complex tasks. The difficulty is increased even more in the case of settings with multiple interacting agents. We apply the artificial homeostatic hormone system (AHHS) approach, which is inspired by the signaling network of unicellular organisms, to control a system of several independently acting agents decentrally. The approach is designed for evaluation-minimal, artificial evolution in order to be applicable to complex modular robotics scenarios. The performance of AHHS controllers is compared with neuroevolution of augmenting topologies (NEAT) in the coupled inverted pendulums benchmark. AHHS controllers are found to be better for multimodular settings. We analyze the evolved controllers with regard to the usage of sensory inputs and the emerging oscillations, and we give a nonlinear dynamics interpretation. The generalization of evolved controllers to initial conditions far from the original conditions is investigated and found to be good. Similarly, the performance of controllers scales well even with module numbers different from the original domain the controller was evolved for. Two reference implementations of a similar controller approach are reported and shown to have shortcomings. We discuss the related work and conclude by summarizing the main contributions of our work.
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http://dx.doi.org/10.1162/artl_a_00058DOI Listing
June 2012

Does Patriline Composition Change over a Honey Bee Queen's Lifetime?

Insects 2012 Sep 13;3(3):857-69. Epub 2012 Sep 13.

Department of Pharmaceutics, Faculty of Pharmacy, Universidade Federal do Rio de Janeiro, Av. Carlos Chagas Filho, 373, CCS, Bloco Bss 31, University City, Rio de Janeiro, RJ, CEP: 21.941-902, Brazil.

A honey bee queen mates with a number of drones a few days after she emerges as an adult. Spermatozoa of different drones are stored in her spermatheca and used for the rest of the queen's life to fertilize eggs. Sperm usage is thought to be random, so that the patriline distribution within a honey bee colony would remain constant over time. In this study we assigned the progeny of a naturally mated honey bee queen to patrilines using microsatellite markers at the queen's age of two, three and four years. No significant changes in patriline distribution occurred within each of two foraging seasons, with samples taken one and five months apart, respectively. Overall and pair-wise comparisons between the three analyzed years reached significant levels. Over the three-year period we found a trend for patrilines to become more equally represented with time. It is important to note that this study was performed with a single queen, and thus individual and population variation in sperm usage patterns must be assessed. We discuss long-term changes in patriline composition due to mixing processes in the queen's spermatheca, following incomplete mixing of different drones' sperm after mating.
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http://dx.doi.org/10.3390/insects3030857DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4553593PMC
September 2012

Inconsistent results of diagnostic tools hamper the differentiation between bee and vespid venom allergy.

PLoS One 2011 15;6(6):e20842. Epub 2011 Jun 15.

Division of Environmental Dermatology and Venerology, Department of Dermatology, Medical University of Graz, Graz, Austria.

Background: Double sensitization (DS) to bee and vespid venom is frequently observed in the diagnosis of hymenoptera venom allergy, but clinically relevant DS is rare. Therefore it is sophisticated to choose the relevant venom for specific immunotherapy and overtreatment with both venoms may occur. We aimed to compare currently available routine diagnostic tests as well as experimental tests to identify the most accurate diagnostic tool.

Methods: 117 patients with a history of a bee or vespid allergy were included in the study. Initially, IgE determination by the ImmunoCAP, by the Immulite, and by the ADVIA Centaur, as well as the intradermal test (IDT) and the basophil activation test (BAT) were performed. In 72 CAP double positive patients, individual IgE patterns were determined by western blot inhibition and component resolved diagnosis (CRD) with rApi m 1, nVes v 1, and nVes v 5.

Results: Among 117 patients, DS was observed in 63.7% by the Immulite, in 61.5% by the CAP, in 47.9% by the IDT, in 20.5% by the ADVIA, and in 17.1% by the BAT. In CAP double positive patients, western blot inhibition revealed CCD-based DS in 50.8%, and the CRD showed 41.7% of patients with true DS. Generally, agreement between the tests was only fair and inconsistent results were common.

Conclusion: BAT, CRD, and ADVIA showed a low rate of DS. However, the rate of DS is higher than expected by personal history, indicating that the matter of clinical relevance is still not solved even by novel tests. Furthermore, the lack of agreement between these tests makes it difficult to distinguish between bee and vespid venom allergy. At present, no routinely employed test can be regarded as gold standard to find the clinically relevant sensitization.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0020842PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3115969PMC
November 2011