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Introduction
I am an integrative biologist interested in using a systems biology approach to improve honey bee health. In addition, I study the effects of pathogens and parasites on bee physiology and behavior to understand the current bee declines.
I also use the honey bee as a model organism to study questions related to animal behavior, physiology, and neurobiology with a particular interest in metabolic homeostasis and the metabolic factors involved in the evolution of social behavior.
Current institution
Additional affiliations
September 2017 - August 2023
September 2015 - August 2017
December 2012 - December 2014
Education
August 2007 - May 2012
August 2003 - May 2007
Publications
Publications (50)
Bee health is declining on a global scale, yet the exact causes and their interactions responsible for the decline remain unknown. To more objectively study bee health, recently biomarkers have been proposed as an essential tool, because they can be rapidly quantified and standardized, serving as a comparable measure across bee species and varying...
Individuals learn about their environment through personal observations or by observing their social conspecifics. This results in two possible learning phenotypes – slow, accurate individual learners and fast, inaccurate social learners. While the costs and benefits of these different learning strategies are recognized, the neurophysiological mech...
Introduction: To maintain energetic homeostasis the energetic state of the individual needs to communicate with appetite regulatory mechanisms on a regular basis. Although hunger levels indicated by the energetic state and appetite levels, the desire for food intake, tend to be correlated, and on their own are well studied, how the two cross-talk a...
Simple Summary
Climate change is associated with warmer and drier weather on average in central California. At the same time, honeybees are being transported from all over the United States to California for the completion of pollination services that ensure increased yields for a variety of crops, resulting in bees experiencing ambient abiotic str...
CRISPR-Cas9 (clustered, regularly interspaced, short palindromic repeats with CRISPR-associated protein 9) is a powerful, versatile, and cost-effective molecular tool that can be used for genetic engineering purposes and beyond ¹ and is especially suited for non-model organisms ² . Effective delivery of this system, however, remains a challenge for...
Background
Honey bees and honeycomb bees are very valuable for wild flowering plants and economically important crops due to their role as pollinators. However, these insects confront many disease threats (viruses, parasites, bacteria and fungi) and large pesticide concentrations in the environment. Varroa destructor is the most prevalent disease t...
Nosema ceranae is a microsporidian that infects Apis species. Recently, natural compounds have been proposed to control nosemosis and reduce its transmission among honey bees. We investigated how ethanolic extract of Tetrigona apicalis's propolis and chito-oligosaccharide (COS) impact the health of N. ceranae-infected Apis dorsata workers. Nosema c...
Simple Summary
RNA-Seq data provide a new chance to find transcriptome variants. We used RNA-Seq data to detect the variants involved in the three different stages (before peak = BP, peak = P, and after peak = AP) of the lactation process in two sheep and two cow breeds. Furthermore, several KEGG pathways and enriched gene ontologies associated wit...
Beekeeping has yet to reach its full potential in terms of productivity in Turkey where it has a relatively large role in the economy. Poor colony health is suspected to be the reason for this, but comprehensive disease monitoring programs are lacking to support this notion. We sampled a total of 115 colonies across five different apiaries througho...
Neonicotinoid pesticide use has increased around the world despite accumulating evidence of their potential detrimental sub-lethal effects on the behaviour and physiology of bees, and its contribution to the global decline in bee health. Whilst flower colour is considered as one of the most important signals for foraging honey bees, the effects of...
Appetite regulation is an important function necessary to maintain energetic balance, but how honey bees accomplish this could vary as they age because they go through a number of behavioral and physiological changes during development. Here, we determine if the amount of trehalose, which is a sugar found in the hemolymph of honey bees, influences...
Nosema ceranae is an intracellular microsporidian pathogen that lives in the midgut ventricular cells of all known honey bee Apis species. We suspect that N. ceranae may also cause energetic stress in the giant honey bee because this parasite is known to disrupt nutrient absorption resulting in energetic stress in the honey bee species Apis mellife...
Nosema ceranae is a large contributing factor to the most recent decline in honey bee health worldwide. Developing new alternative treatments against N. ceranae is particularly pressing because there are few treatment options available and therefore the risk of increased antibiotic resistance is quite high. Recently, natural products have demonstra...
Use of chemicals, such as alarm pheromones, for rapid communication with conspecifics is widespread throughout evolutionary history. Such chemicals are particularly important for social insects, such as the honeybee ( Apis mellifera ), because they are used for collective decision-making, coordinating activities and self-organization of the group....
The exponential growth in knowledge has resulted in a better understanding of the lactation process in a wide variety of animals. However, the underlying genetic mechanisms are not yet clearly known. In order to identify the mechanisms involved in the lactation process, various mehods, including meta-analysis, weighted gene co-express network analy...
Insects, due to their small size, have limited energy storage space, but they also have high metabolic rate, so their hemolymph sugars are incredibly dynamic and play a number of important physiological functional roles in maintaining energetic homeostasis. In contrast to vertebrates, trehalose is generally the primary sugar found in insect hemolym...
Collective decision making is essential for multicellular and self-organized society coordination, but how this occurs when most of the individuals have limited knowledge of the external environment remains elusive. Using empirical data to inform a neuroscience-based firing-rate model, we found that integration of negative feedback and network dyna...
The recent decline of European honey bees (Apis mellifera) has prompted a surge in research into their chemical environment, including chemicals produced by bees, as well as chemicals produced by plants and derived from human activity that bees also interact with. This study sought to develop a novel approach to passively sampling honey bee hives u...
Insects have rapidly changing energy demands, so they primarily rely on hemolymph and other carbohydrates to carry out life activities. However, how gustatory responsiveness and hemolymph sugar levels coordinate with one another to maintain energetic homeostasis in insects remains largely unknown for the highly social honeybee that goes through lar...
The importance of not only honey bees (Apis mellifera) but also other non-managed bee species and their pollination services has come to light with their recently reported declines. One contributing factor in these declines is thought to be sub-lethal exposure to neonicotinoid insecticides such as thiacloprid. However, current government regulatory...
The importance of not only honey bees (Apis mellifera) but also other non-managed bee species and their pollination services has come to light with their recently reported declines. One contributing factor in these declines is thought to be sub-lethal exposure to neonicotinoid insecticides such as thiacloprid. However, current government regulatory...
[This corrects the article DOI: 10.1371/journal.pone.0213249.].
Honey bee (Apis mellifera) health has been severely impacted by multiple environmental stressors including parasitic infection, pesticide exposure, and poor nutrition. The decline in bee health is therefore a complex multifactorial problem which requires a holistic investigative approach. Within the exposome paradigm, the combined exposure to the e...
Geography type and randomized sample identifiers.
(DOCX)
A list of primers used for sq-PCR analyses for Nosema ceranae and Nosema apis.
MITOC-F, MITOC-R, APIS-F, APIS-R are taken from Hamiduzzaman, et al. (2010)[35] and RpS5-F, RpS5-R are taken from reference Thompson et al. (2007)[69].
(DOCX)
Raw data of the study for public access.
(XLSX)
Relative ion abundances of detected xenobiotics (log2 normalized for scaling).
Relative ion abundances of detected xenobiotics (log2 normalized for scaling). Data is represented by medians and error bars represent interquartile ranges for each xenobiotic. For each category, there was no significant association between the relative level of exposure...
2x2 contingency table.
The case and controls groups did not vary significantly based on ion abundance greater than or less than the combined median ion abundance (24.37, Log2 normalized).
(DOCX)
2x2 contingency tables.
A. Ion abundance greater than or less than the median ion abundance stratified by chemical category. B. 2x2 contingency tables. Ion abundance greater than or less than the median ion abundance stratified by chemical category.
(DOCX)
Mode of action for the most common xenobiotics identified.
(DOCX)
Nosema ceranae is now considered to be an emerging infectious disease of the European honey bee Apis mellifera. Only one antibiotic, Fumagillin, is commercially available to combat Nosema infections. This antibiotic treatment is banned from use in Europe and elsewhere there is a high probability for antibiotic resistance to develop. We are therefor...
A pilot study was conducted to determine if exposome profiles of honey bees (Apis mellifera) are associated with Nosema ceranae infection and whether xenobiotic exposures effect changes in known biological pathways of bees. Thirty stationary hives were selected from seven apiaries representing urban and suburban geographies. Foraging bees were harv...
Host-pathogen coevolution leads to reciprocal adaptations, allowing pathogens to increase host exploitation or hosts to minimise costs of infection. As pathogen resistance is often associated with considerable costs, tolerance may be an evolutionary alternative. Here, we examined the effect of two closely related and highly host dependent intracell...
Nosema ceranae, an emerging pathogen of the western honeybee (Apis mellifera), is implicated in recent pollinator losses and causes severe energetic stress. However, whether precocious foraging and accelerated behavioural maturation in infected bees are caused by the infection itself or via indirect energetic stress remains unknown. Using a combina...
Impulsivity, the widespread preference for a smaller and more immediate reward over a larger and more delayed reward, is known to vary across species, and the metabolic and social hypotheses present contrasting explanations for this variation. However, this presents a paradox for an animal such as the honeybee, which is highly social, yet has a hig...
The energetic state of an individual is a fundamental driver of its behavior. However, an individual in a eusocial group such as the honeybees is subject to the influence of both the individual and the colony energetic states. As these two states are normally coupled, it has led to the predominant view that behaviors, such as foraging, are dictated...
Animals are sensitive to risk or the variability of a reward distribution, and the energy budget rule of risk sensitivity theory predicts that it is adaptive for an animal to be risk averse when it is on a positive energy budget and to be risk prone when it is on a negative budget, because the utility of a potential large reward is much higher in t...
Nosema ceranae is a relatively new and widespread parasite of the western honeybee Apis mellifera that provokes a new form of nosemosis. In comparison to Nosema apis, which has been infecting the honeybee for much longer, N. ceranae seems to have co-evolved less with this host, causing a more virulent disease. Given that N. apis and N. ceranae are...
Parasites by drawing nutrition from their hosts can exert an energetic stress on them. Honeybee foragers with their high metabolic demand due to flight are especially prone to such a stress when they are infected. We hypothesized that infection by the microsporidian gut parasite Nosema ceranae can lower the hemolymph sugar level of an individual fo...
Infection by a parasite often induces behavioural changes in the host and these changes may benefit either the host or the parasite. However, whether these changes are active host defence mechanisms or parasitic manipulations or simply incidental byproducts of the infection is not always clear. It has been suggested that understanding the proximate...
Parasites are dependent on their hosts for energy to reproduce and can exert a significant nutritional stress on them. The microsporidian Nosema ceranae is a relatively new parasite in the honeybee Apis mellifera that is replacing Nosema apis throughout the world. Using Proboscis Extension Response (PER) and feeding experiments, we show that bees i...
Parasites are dependent on their hosts for energy to reproduce and can exert a significant nutritional stress on them. Energetic demand placed on the host is especially high in cases where the parasite-host complex is less co-evolved. The higher virulence of the newly discovered honeybee pathogen, Nosema ceranae, which causes a higher mortality in...
Questions
Questions (2)
I have done some extensive searching to find a lab with an electrochemical detector in or around Halle (Saale) Germany, which will be crucial to analyze honeybee brains that I plan to collect this summer. I have tried using a mass spec before and the sensitivity was not quite adequate to analyze the neurotransmitters of honeybee brains. The closest electrochemical detector I have been able to locate is in the Netherlands. Any leads in which I can follow up on is greatly appreciated.
I am aware of how to extract and measure insect hormones from the hemolymph and the brain, but I would ideally like to quantify the total hormone present in the insect. I am assuming that this extraction method would involve crushing the entire individual and then possibly spinning the contents down to avoid all of the solid material.
