Nigel Raine | University of Guelph (original) (raw)

Papers by Nigel Raine

Frontiers in Ecology and the Environment, 2013

Pressures on pollinators AJ Vanbergen et al. www.frontiersinecology.org

1. The ability to forage and return home is essential to the success of bees as both foragers and... more 1. The ability to forage and return home is essential to the success of bees as both foragers and pollinators. Pesticide exposure may cause behavioural changes that interfere with these processes, with consequences for colony persistence and delivery of pollination services. 2. We investigated the impact of chronic exposure (5–43 days) to field-realistic levels of a neonicotinoid insecticide (2Á4 ppb thiamethoxam) on foraging ability, homing success and colony size using radio frequency identification (RFID) technology in free-flying bumblebee colonies. 3. Individual foragers from pesticide-exposed colonies carried out longer foraging bouts than untreated controls (68 vs. 55 min). Pesticide-exposed bees also brought back pollen less frequently than controls indicating reduced foraging performance. 4. A higher proportion of bees from pesticide-exposed colonies returned when released 1 km from their nests; this is potentially related to increased orientation experience during longer foraging bouts. We measured no impact of pesticide exposure on homing ability for bees released from 2 km, or when data were analysed overall. 5. Despite a trend for control colonies to produce more new workers earlier, we found no overall impacts of pesticide exposure on whole colony size. 6. Synthesis and applications. This study shows that field-realistic neonicotinoid exposure can have impacts on both foraging ability and homing success of bumblebees, with implications for the success of bumblebee colonies in agricultural landscapes and their ability to deliver crucial pollination services. Pesticide risk assessments should include bee species other than honeybees and assess a range of behaviours to elucidate the impact of sublethal effects. This has relevance for reviews of neonicotinoid risk assessment and usage policy worldwide .

Biological Reviews

Animal personalities or behavioural syndromes are consistent and/or correlated behaviours across ... more Animal personalities or behavioural syndromes are consistent and/or correlated behaviours across two or more situations within a population. Social insect biologists have measured consistent individual variation in behaviour within and across colonies for decades. The goal of this review is to illustrate the ways in which both the study of social insects and of behavioural syndromes has overlapped, and to highlight ways in which both fields can move forward through the synergy of knowledge from each. Here we, (i) review work to date on behavioural syndromes (though not always referred to as such) in social insects, and discuss mechanisms and fitness effects of maintaining individual behavioural variation within and between colonies; (ii) summarise approaches and principles from studies of behavioural syndromes, such as trade-offs, feedback, and statistical methods developed specifically to study behavioural consistencies and correlations, and discuss how they might be applied specif...

Scientific reports, 2016

The capacity to explore soft tissue structures in detail is important in understanding animal phy... more The capacity to explore soft tissue structures in detail is important in understanding animal physiology and how this determines features such as movement, behaviour and the impact of trauma on regular function. Here we use advances in micro-computed tomography (micro-CT) technology to explore the brain of an important insect pollinator and model organism, the bumblebee (Bombus terrestris). Here we present a method for accurate imaging and exploration of insect brains that keeps brain tissue free from trauma and in its natural stereo-geometry, and showcase our 3D reconstructions and analyses of 19 individual brains at high resolution. Development of this protocol allows relatively rapid and cost effective brain reconstructions, making it an accessible methodology to the wider scientific community. The protocol describes the necessary steps for sample preparation, tissue staining, micro-CT scanning and 3D reconstruction, followed by a method for image analysis using the freeware SPIE...

Recent concern over global pollinator declines has led to considerable research on the effects of... more Recent concern over global pollinator declines has led to considerable research on the effects of pesticides on bees. Although pesticides are typically not encountered at lethal levels in the field, there is growing evidence indicating that exposure to field-realistic levels can have sublethal effects on bees, affecting their foraging behaviour, homing ability and reproductive success. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants, but until now research on pesticide effects has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence to our knowledge that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Bumblebee colonies exposed to a neonicotinoid pesticide provided lower visitation rates to apple trees and collected pollen less often. Most importantly, these pesticide-exposed colonies produced apples containing fewer seeds, demonstrating a reduced delivery of pollination services. Our results also indicate that reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour, but most likely due to effects at the colony level. These findings show that pesticide exposure can impair the ability of bees to provide pollination services, with important implications for both the sustained delivery of stable crop yields and the functioning of natural ecosystems.

Scientific reports, 2015

Bumblebees are exposed to pesticides applied for crop protection while foraging on treated plants... more Bumblebees are exposed to pesticides applied for crop protection while foraging on treated plants, with increasing evidence suggesting that this sublethal exposure has implications for pollinator declines. The challenges of navigating and learning to manipulate many different flowers underline the critical role learning plays for the foraging success and survival of bees. We assessed the impacts of both acute and chronic exposure to field-realistic levels of a widely applied neonicotinoid insecticide, thiamethoxam, on bumblebee odour learning and memory. Although bees exposed to acute doses showed conditioned responses less frequently than controls, we found no difference in the number of individuals able to learn at field-realistic exposure levels. However, following chronic pesticide exposure, bees exposed to field-realistic levels learnt more slowly and their short-term memory was significantly impaired following exposure to 2.4 ppb pesticide. These results indicate that field-re...

Nature Precedings

Despite the widespread assumption that the learning abilities of animals are adapted to the parti... more Despite the widespread assumption that the learning abilities of animals are adapted to the particular environments in which they operate, the quantitative effects of learning performance on fitness remain virtually unknown. Here we evaluate the learning performance of bumblebees (Bombus terrestris) from multiple colonies in an ecologically relevant associative learning task under laboratory conditions, before testing the foraging performance of the same colonies under the field conditions. We demonstrate that variation in learning speed among bumblebee colonies is directly correlated with foraging performance, a robust fitness measure, under natural conditions. Colonies vary in learning speed by a factor of nearly 5, with the slowest learning colonies collecting 40% less nectar than the fastest learning colonies. Such a steep fitness function suggests strong selection for higher learning speed in bumblebees. Demonstrating the adaptive value of differences in learning performance under the real conditions in which animals function represents a major step towards understanding how cognitive abilities of animals are tuned to their environment.

Integrated Environmental Assessment and Management, 2015

Global declines of bumble bees and other pollinator populations are of concern because of their c... more Global declines of bumble bees and other pollinator populations are of concern because of their critical role for crop production and maintenance of wild plant biodiversity. Although the consensus among scientists is that the interaction of many factors, including habitat loss, forage scarcity, diseases, parasites, and pesticides potentially plays a role in causing these declines, pesticides have received considerable public attention and scrutiny. In response, regulatory agencies have introduced more stringent pollinator testing requirements for registration and re-registration of pesticides, to ensure the risks to pollinators are minimized. In this context, guidelines for testing bumble bees (Bombus spp.) in regulatory studies are not yet available and there is a pressing need to develop suitable protocols for routine higher tier studies with these non-Apis, social bees. To meet this need, Bayer CropScience LP, Syngenta Crop Protection LLC US, and Valent U.S.A. Corporation organized a workshop bringing together a group of global experts on bumble bee behavior, ecology and ecotoxicology to discuss and develop draft protocols for both semi-field (Tier II) and field (Tier III) studies. The workshop was held May 8-9, 2014 at the Bayer Bee Care Center, North Carolina. The participants represented academic, consulting, and industry scientists from Europe, Canada, USA, and Brazil. The workshop identified a clear protection goal and generated proposals for basic experimental designs, relevant measurements and endpoints for both semi-field (tunnel) and field tests. These initial recommendations are intended to form the basis of discussions to help advance the development of appropriate protocol guidelines. This article is protected by copyright. All rights reserved.

Contemporary Topics in Entomology, 2009

Mkomazi Game Reserve has never been noted for large populations of large mam- mals but the divers... more Mkomazi Game Reserve has never been noted for large populations of large mam- mals but the diversity of species is as great as in any other east African protected area. The size criterion defining a large mammal must, ultimately, be arbitrary. In ecological terms, individual size correlates with individual contribution to the rate at which ecological processes occur. The threshold

Biology Letters, 2009

The immune response affects learning and memory in insects. Given this and the known fitness cost... more The immune response affects learning and memory in insects. Given this and the known fitness costs of both the immune system and learning, does an evolutionary trade-off exist between these two systems? We tested this by measuring the learning ability of 12 bumble-bee (Bombus terrestris) colonies in a free-flying paradigm. We then tested their immune response using the zone of inhibition assay. We found a positive relationship between colony learning performance and immune response, that is, fast-learning colonies also show high levels of antimicrobial activity. We conclude that there is no a priori reason to demand an evolutionary relationship between two traits that are linked physiologically.

Nature, 2015

Two studies provide evidence that bees cannot taste or avoid neonicotinoid pesticides, and that e... more Two studies provide evidence that bees cannot taste or avoid neonicotinoid
pesticides, and that exposure to treated crops affects reproduction in solitary bees
as well as bumblebee colony growth and reproduction.

Functional Ecology, 2014

1. Insect pollination is a vital ecosystem service that maintains biodiversity and sustains agric... more 1. Insect pollination is a vital ecosystem service that maintains biodiversity and sustains agricultural crop yields. Social bees are essential insect pollinators, so it is concerning that their populations are in global decline. 2. Although pesticide exposure has been implicated as a possible cause for bee declines, we currently have a limited understanding of the risk these chemicals pose. Whilst environmental exposure to pesticides typically has non-lethal effects on individual bees, recent reports suggest that sublethal exposure can affect important behavioural traits such as foraging. However, at present, we know comparatively little about how natural foraging behaviour is impaired and the relative impacts of acute and chronic effects. 3. Using Radio-Frequency Identification (RFID) tagging technology, we examined how the day-to-day foraging patterns of bumblebees (Bombus terrestris) were affected when exposed to either a neonicotinoid (imidacloprid) and/or a pyrethroid (k-cyhalothrin) independently and in combination over a four-week period. This is the first study to provide data on the impacts of combined and individual pesticide exposure on the temporal dynamics of foraging behaviour in the field over a prolonged period of time. 4. Our results show that neonicotinoid exposure has both acute and chronic effects on overall foraging activity. Whilst foragers from control colonies improved their pollen foraging performance as they gained experience, the performance of bees exposed to imidacloprid became worse: chronic behavioural impairment. We also found evidence, suggesting that pesticide exposure can change forager preferences for the flower types from which they collect pollen. 5. Our findings highlight the importance of considering prolonged exposure (which happens in the field) when assessing the risk that pesticides pose to bees. The effects of chronic pesticide exposure could have serious detrimental consequences for both colony survival and also the pollination services provided by these essential insect pollinators.

Nature, 2012

Reported widespread declines of wild and managed insect pollinators have serious consequences for... more Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production 1-3 . Bees contribute approximately 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations 4-6 . Recent studies have implicated the role of pesticides in these declines, as exposure to these chemicals has been associated with changes in bee behaviour 7-11 and reductions in colony queen production 12 . However, the key link between changes in individual behaviour and the consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of many individual workers. Thus, although field-level pesticide concentrations can have subtle or sublethal effects at the individual level 8 , it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means that bees are exposed to numerous pesticides when foraging 13-15 , yet the possible combinatorial effects of pesticide exposure have rarely been investigated . Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concentrations that could approximate field-level exposure impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success. We found that worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with observed knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail.