Insect psychoneuroimmunology: Immune response reduces learning in protein starved bumblebees (Bombus terrestris)

Riddell, Carolyn; Mallon, Eamonn B.

doi:10.1016/j.bbi.2005.06.008

Cited by 66 publications

(71 citation statements)

References 15 publications

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“…An altered immune system as discussed above [15,53] could potentially explain the lower learning rate in Nosema-inoculated bumblebees, suggesting that ingestion of spores solely may be stressful for bumblebees. The low infectivity of bumblebees is intriguing given our preliminary tests showed that 60% of the inoculated bees became infected.…”

Section: Discussionmentioning

confidence: 99%

“…At the same time, it is noted that the impact of parasites on learning may become more pronounced in field conditions as indicated by a semi-field study using free-flying bumblebees [51]. The mechanisms underlying pathogen-driven reductions in learning or memory are still relatively poorly understood, but potentially involve interactions between the immune system and the nervous system [14][15][16]. Previous studies have shown that parasite challenge can induce various alterations of the immune system of bees (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies have shown that parasite challenge can induce various alterations of the immune system of bees (e.g. [52,53]), and this, even without actual successful infection and production of spores, can impair the learning and memory of bees as shown by stimulating the immune system of honeybees and bumblebees with non-pathogenic elicitors, lipopolysaccharides [14,15,51].…”

Section: Discussionmentioning

confidence: 99%

“…Acting as nicotinic acetylcholine receptor (nAChR) agonists [10], exposure to very low levels of neonicotinoids can disrupt normal function of neurons in the bee brain [11,12] and lead to disruptions in learning and memory [8,13]. Diseases and parasites disrupt bee behaviour and learning potentially via altering the immune system which is linked to the nervous system [14][15][16]. There is increasing evidence indicating that interactive effects particularly between insecticides and parasites/diseases may have detrimental impacts on bees (e.g.…”

Section: Introductionmentioning

confidence: 99%

“…This parasite has been associated with colony losses in some areas in Europe [30,31] and has also recently been found in wild bumblebees, where it may cause significant mortality [21], though not always [32]. We use the proboscis extension response (PER) assay, a widely used method for studying learning and memory in honeybees [33,34] and more recently also in bumblebees [13,15,35,36], to assess potential effects of the aforementioned stress factors on olfactory associative learning and memory.…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Piiroinen¹,

Goulson²

2016

Proc. R. Soc. B.

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Learning and memory are crucial functions which enable insect pollinators to efficiently locate and extract floral rewards. Exposure to pesticides or infection by parasites may cause subtle but ecologically important changes in cognitive functions of pollinators. The potential interactive effects of these stressors on learning and memory have not yet been explored. Furthermore, sensitivity to stressors may differ between species, but few studies have compared responses in different species. Here, we show that chronic exposure to fieldrealistic levels of the neonicotinoid clothianidin impaired olfactory learning acquisition in honeybees, leading to potential impacts on colony fitness, but not in bumblebees. Infection by the microsporidian parasite Nosema ceranae slightly impaired learning in honeybees, but no interactive effects were observed. Nosema did not infect bumblebees (3% infection success). Nevertheless, Nosema-treated bumblebees had a slightly lower rate of learning than controls, but faster learning in combination with neonicotinoid exposure. This highlights the potential for complex interactive effects of stressors on learning. Our results underline that one cannot readily extrapolate findings from one bee species to others. This has important implications for regulatory risk assessments which generally use honeybees as a model for all bees.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Piiroinen¹,

Goulson²

2016

Proc. R. Soc. B.

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The Effect of Non‐Self Genes on the Behaviour of Hosts

Wedell

2019

Genes and Behaviour

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Quantitative genetics of learning ability and resistance to stress inDrosophila melanogaster

Népoux

Babin

Haag

et al. 2015

Ecology and Evolution

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Even though laboratory evolution experiments have demonstrated genetic variation for learning ability, we know little about the underlying genetic architecture and genetic relationships with other ecologically relevant traits. With a full diallel cross among twelve inbred lines of Drosophila melanogaster originating from a natural population (0.75 < F < 0.93), we investigated the genetic architecture of olfactory learning ability and compared it to that for another behavioral trait (unconditional preference for odors), as well as three traits quantifying the ability to deal with environmental challenges: egg-to-adult survival and developmental rate on a low-quality food, and resistance to a bacterial pathogen. Substantial additive genetic variation was detected for each trait, highlighting their potential to evolve. Genetic effects contributed more than nongenetic parental effects to variation in traits measured at the adult stage: learning, odorant perception, and resistance to infection. In contrast, the two traits quantifying larval tolerance to low-quality food were more strongly affected by parental effects. We found no evidence for genetic correlations between traits, suggesting that these traits could evolve at least to some degree independently of one another. Finally, inbreeding adversely affected all traits.

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Insect psychoneuroimmunology: Immune response reduces learning in protein starved bumblebees (Bombus terrestris)

Cited by 66 publications

References 15 publications

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees

The Effect of Non‐Self Genes on the Behaviour of Hosts

Quantitative genetics of learning ability and resistance to stress inDrosophila melanogaster

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