<i>Nosema ceranae</i> parasitism impacts olfactory learning and memory and neurochemistry in honey bees <i>(Apis mellifera)</i>

Gage, Stephanie L.; Kramer, Catherine; Calle, Samantha; Carroll, Mark J.; Heien, Michael L.; DeGrandi-Hoffman, Gloria

doi:10.1242/jeb.161489

Cited by 38 publications

(44 citation statements)

References 77 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The results from the PER assays in this work are consistent with those of two previous studies showing no effects of N. apis or N. ceranae infections on honey bee learning and memory using the PER assay [16,53]. Conversely, Gage et al [54] showed that N. ceranae negatively impacts PER in honey bees. While Gage et al [54] used the same level of inoculum, they tested 7-to 15-day-old bees versus 13-to 19-day-old bees in this study.…”

Section: Discussionsupporting

confidence: 92%

See 1 more Smart Citation

Effect of Immune Inducers on Nosema ceranae Multiplication and Their Impact on Honey Bee (Apis mellifera L.) Survivorship and Behaviors

Valizadeh

Guzmán-Novoa

Goodwin

2020

Insects

View full text Add to dashboard Cite

Nosema disease is a major disease of honey bees caused by two species of microsporidia, Nosema apis and N. ceranae. Current control involves using antibiotics, which is undesirable because of possible antibiotic resistance and contamination. In this study, flagellin, zymosan, chitosan, and peptidoglycan were investigated as alternatives for controlling N. ceranae infections and for their effect on bee survivorship and behaviors. Chitosan and peptidoglycan significantly reduced the infection, and significantly increased survivorship of infected bees, with chitosan being more effective. However, neither compound altered the bees’ hygienic behavior, which was also not affected by the infection. Chitosan significantly increased pollen foraging and both compounds significantly increased non-pollen foraging compared to healthy and infected bees. Memory retention, evaluated with the proboscis extension reflex assay, was temporarily impaired by chitosan but was not affected by peptidoglycan, nor was it affected by N. ceranae infection compared to the non-infected bees. This study indicates that chitosan and peptidoglycan provide benefits by partially reducing N. ceranae spore numbers while increasing survivorship compared to N. ceranae infected bees. Also, chitosan and peptidoglycan improved aspects of foraging behavior even more than in healthy bees, showing that they may act as stimulators of important honey bee behaviors.

show abstract

Section: Discussionsupporting

confidence: 92%

“…Conversely, Gage et al [54] showed that N. ceranae negatively impacts PER in honey bees. While Gage et al [54] used the same level of inoculum, they tested 7-to 15-day-old bees versus 13-to 19-day-old bees in this study. Thus, the age of the bees could be having an impact on the results, warranting further investigation.…”

Section: Discussionmentioning

confidence: 97%

Effect of Immune Inducers on Nosema ceranae Multiplication and Their Impact on Honey Bee (Apis mellifera L.) Survivorship and Behaviors

Valizadeh

Guzmán-Novoa

Goodwin

2020

Insects

View full text Add to dashboard Cite

show abstract

“…The details of the amino acid analyses on individual brains are described in Gage et al (2018). In brief, conventional acid hydrolysis with chloroformate derivatization was used to quantify all amino acids, with the exceptions of tryptophan, cysteine, and arginine.…”

Section: Amino Acid Analysis Of Brain Tissue and Pollenmentioning

confidence: 99%

“…One may also consider the parasitic-nature of N. ceranae (Vidau et al, 2014;Mayack et al, 2015;Gage et al, 2018). There are host-parasite examples where parasites use nutrients from hosts to fuel replication (Zuzarte-Luís and Mota, 2018).…”

Section: Effects Of Parasitic Stress From Nosema Ceranaementioning

confidence: 99%

Pollen Alters Amino Acid Levels in the Honey Bee Brain and This Relationship Changes With Age and Parasitic Stress

et al. 2020

Self Cite

View full text Add to dashboard Cite

Pollen nutrition is necessary for proper growth and development of adult honey bees. Yet, it is unclear how pollen affects the honey bee brain and behavior. We investigated whether pollen affects amino acids in the brains of caged, nurse-aged bees, and what the behavioral consequences might be. We also tested whether parasitic stress altered this relationship by analyzing bees infected with prevalent stressor, Nosema ceranae. Levels of 18 amino acids in individual honey bee brains were measured using Gas Chromatography -Mass Spectrometry at two different ages (Day 7 and Day 11). We then employed the proboscis extension reflex to test odor learning and memory. We found that the honey bee brain was highly responsive to pollen. Many amino acids in the brain were elevated and were present at higher concentration with age. The majority of these amino acids were non-essential. Without pollen, levels of amino acids remained consistent, or declined. Nosema-infected bees showed a different profile. Infection altered amino acid levels in a pollen-dependent manner. The majority of amino acids were lower when pollen was given, but higher when pollen was deprived. Odor learning and memory was not affected by feeding pollen to uninfected bees; but pollen did improve performance in Nosema-infected bees. These results suggest that pollen in early adulthood continues to shape amino acid levels in the brain with age, which may affect neural circuitry and behavior over time. Parasitic stress by N. ceranae modifies this relationship revealing an interaction between infection, pollen nutrition, and behavior.

show abstract

“…By exploiting the host cell's machinery to obtain resources, N. ceranae infection affects vital functions and modifies the host's immune response, ultimately causing cell lysis [21] and digestive disorders, provoking changes in vital functions and modifying the host's immune response, and significantly compromising the survival of the infected bee [22][23][24][25][26][27][28][29]. This pathogen also affects aspects of honey bee neurobiology, such as olfaction, learning and memory [30], and the orientation and homing skills of workers [31], accelerating bee aging and their related tasks [32][33][34].…”

Section: Introductionmentioning

confidence: 99%

Age and Method of Inoculation Influence the Infection of Worker Honey Bees (Apis mellifera) by Nosema ceranae

Urbieta-Magro

Higes

Meana

et al. 2019

Insects

View full text Add to dashboard Cite

The microsporidian parasite Nosema ceranae is a highly prevalent, global honey bee pathogen. Apis mellifera is considered to be a relatively recent host for this microsporidia, which raises questions as to how it affects its host’s physiology, behavior and longevity, both at the individual and colony level. As such, honey bees were inoculated with fresh purified spores of this pathogen, both individually (Group A) or collectively (Group B) and they were studied from 0 to 15 days post-emergence (p.e.) to evaluate the effect of bee age and the method of inoculation at 7 days post-infection. The level of infection was analyzed individually by qPCR by measuring the relative amount of the N. ceranae polar tubule protein 3 (PTP3) gene. The results show that the bee’s age and the method of infection directly influence parasite load, and thus, early disease development. Significant differences were found regarding bee age at the time of infection, whereby the youngest bees (new-born and 1 day p.e.) developed the highest parasite load, with this load decreasing dramatically in bees infected at 2 days p.e. before increasing again in bees infected at 3–4 days p.e. The parasite load in bees infected when older than 4 days p.e. diminished as they aged. When the age cohort data was pooled and grouped according to the method of infection, a significantly higher mean concentration and lower variation in N. ceranae infection was evident in Group A, indicating greater variation in experimental infection when spores were administered collectively to bees through their food. In summary, these data indicate that both biological and experimental factors should be taken into consideration when comparing data published in the literature.

show abstract

Nosema ceranae parasitism impacts olfactory learning and memory and neurochemistry in honey bees (Apis mellifera)

Cited by 38 publications

References 77 publications

Effect of Immune Inducers on Nosema ceranae Multiplication and Their Impact on Honey Bee (Apis mellifera L.) Survivorship and Behaviors

Effect of Immune Inducers on Nosema ceranae Multiplication and Their Impact on Honey Bee (Apis mellifera L.) Survivorship and Behaviors

Pollen Alters Amino Acid Levels in the Honey Bee Brain and This Relationship Changes With Age and Parasitic Stress

Age and Method of Inoculation Influence the Infection of Worker Honey Bees (Apis mellifera) by Nosema ceranae

Contact Info

Product

Resources

About