Fig 5 - available via license: Creative Commons Attribution 4.0 International
Content may be subject to copyright.
Transfer diagrams showing the flow between infection classes separately for the honey bees, shown in (a), and mites, shown in (b). Justification of the different components and their functional forms is given in the text
Source publication
Viral diseases of honey bees are important economically and ecologically and have been widely modelled. The models reflect the fact that, in contrast to the typical case for vertebrates, invertebrates cannot acquire immunity to a viral disease, so they are of SIS or (more often) SI type. Very often, these diseases may be transmitted vertically as w...
Context in source publication
Context 1
... overtly infected, bees and mites remain overtly infected throughout their life. Figure 5a and b shows the transfer between these classes separately for the bees and the mites and should be used as an aide memoire as we now describe the demographic and infection processes that we combine together to describe viral infection within the honey-bee and mite ecosystem. Honey-bee production The infection status of adult bees emerging from brood cells will clearly impact the model dynamics. ...
Similar publications
New Zealand’s temperate climate and bountiful flora are well suited to managed honey bees, and its geographic isolation and strict biosecurity laws have made sure that some pests and diseases affecting bees elsewhere are not present. Nevertheless, given the importance of pollination and high-value export honey to the economy, New Zealand began syst...
Citations
... Since then, numerous mathematical models (such as [17,[21][22][23] and some references therein) continue to build on [20]. In 2021, Britton and White presented a mathematical model that describe how compartmental structure for infection impacts the disease dynamics observed, in particular on DWV vectored by varroa mites [24]. Messan et al. (2021) uses stage-structure delay model to investigate the role mites growth on honeybee health and population dynamics. ...
In this paper, a mechanistic model of Acute Bee Paralysis Virus (ABPV) transmission is designed and analyzed. The qualitative behavior of honeybee-pathogen and honeybee-pathogen-mite interactions sub-models revealed the existence of backward bifurcation. It is shown that whenever the survivability of a newly hatched egg is guaranteed, both the disease-free and endemic equilibria of the sub-models are globally asymptotically stable. Sensitivity and uncertainty analyses have shown that egg-laying, viral ingestion and deposition rates are the most influential parameters that drive ABPV infection. Suggesting that intervention strategies that focus on how to manage these rates are required for effective control. The combination of disinfection and fumigation of hives, using optimal control analysis, is shown to be the most effective strategy for controlling the spread of ABPV infection. In addition, disinfection alone is found to be the most cost-effective strategy. Finally, an extended model that incorporates mite migration and parasitism is formulated and simulated. The results have shown that mite migration weakens the colony and spacing hives to the farthest distance a forager can reach strengthen the colony. It is also shown that parasitism contributes towards colony collapse, however, fumigation strategy reduces honeybee mortality due to parasitism.
... Covert infection could explain why our apparently "healthy" individuals are more variable in terms of mobility than the infected ones, with potentially bigger differences between D. magna that are actually uninfected and patent-infected individuals. In theoretical work, there are interesting studies on various epidemiological models (like SEIR) that could be adapted by taking into account the additional category of exposed individuals (e.g., Sorrell et al., 2009;Britton & Jane White, 2021). ...
Parasites are omnipresent, and their eco-evolutionary significance has aroused much interest from scientists. Parasites may affect their hosts in many ways with changes in density, appearance, behaviour and energy content, likely to modify their value to predators (profitability) within the optimal foraging framework. Consequently, parasites could impact predators' diet and the trophic links through food webs. Here, we investigate the consequences of the infection by the iridovirus Daphnia iridescent virus 1 (DIV-1) on the reproductive success, mortality, appearance, mobility, and biochemical composition of water fleas (Daphnia magna), a widespread freshwater crustacean. We do predation tests and compare search time, handling time and feeding preference between infected and uninfected Daphnia when preyed upon by Notonecta sp., a common aquatic insect. Our findings show that infection does not change fecundity but reduces lifespan and thereby constrains fitness. Infected Daphnia show reduced mobility and increased color reflectance in the UV and visible domains, which potentially affects their appearance and thus vulnerability to predators. Infection increases body size and the amount of proteins but does not affect carbohydrate and lipid contents. Although infected Daphnia are longer to handle, they are preferred over uninfected individuals by aquatic insects. Taken together, our findings show that DIV-1 infection could make Daphnia more profitable to predators (24% energy increase), a positive effect that should be balanced with a lower availability due to the higher mortality of infected specimens. We also highlight that exposure to infection in asymptomatic individuals leads to ecological characteristics that differ from both healthy and symptomatic infected individuals.
... Covert infection could explain why our apparently "healthy" individuals are more variable in terms of mobility than the infected ones, with potentially bigger differences between D. magna that are actually uninfected and patent-infected individuals. In theoretical work, there are interesting studies on various epidemiological models (like SEIR) that could be adapted by taking into account the additional category of exposed individuals (e.g., Sorrell et al., 2009;Britton & Jane White, 2021). ...
Parasites are omnipresent, and their eco-evolutionary significance has aroused much interest from scientists. Parasites may affect their hosts in many ways with changes in density, appearance, behaviour and energy content, likely to modify their value to predators (profitability) within the optimal foraging framework. Consequently, parasites could impact predators’ diet and the trophic links through food webs. Here, we investigate the consequences of the infection by the iridovirus Daphnia iridescent virus 1 (DIV-1) on the reproductive success, mortality, appearance, mobility, and biochemical composition of water fleas ( Daphnia magna ), a widespread freshwater crustacean. We do predation tests and compare search time, handling time and feeding preference between infected and uninfected Daphnia when preyed upon by Notonecta sp., a common aquatic insect. Our findings show that infection does not change fecundity but reduces lifespan and thereby constrains fitness. Infected Daphnia show reduced mobility and increased color reflectance in the UV and visible domains, which potentially affects their appearance and thus vulnerability to predators. Infection increases body size and the amount of proteins but does not affect carbohydrate and lipid contents. Although infected Daphnia are longer to handle, they are preferred over uninfected individuals by aquatic insects. Taken together, our findings show that DIV-1 infection could make Daphnia more profitable to predators (24% energy increase), a positive effect that should be balanced with a lower availability due to the higher mortality of infected specimens. We also highlight that exposure to infection in asymptomatic individuals leads to ecological characteristics that differ from both healthy and symptomatic infected individuals.
Recommender: Luis Schiesari
Reviewers: Thierry De Meeus and Eglantine Mathieu-Bégné
Cite as: Prosnier L., N. Loeuille, F.D. Hulot, D. Renault, C. Piscart, B. Bicocchi, M, Deparis, M. Lam, & V. Médoc. (2023).
Parasites make hosts more profitable but less available to predators. BioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.02.08.479552
... The hallmark of Murray's work on disease dynamics, such as HIV, has been to gain insight from realistic models, tailored to the specific details that can so often affect outcomes. Britton and White (2021) show how the inclusion of multiple infection classes in a honey-bee-mite-virus system is key to our understanding of spontaneous transitions between disease states as bees and mites move from covertly to overtly infected states. These distinct infection classes then play a key role in governing disease outcomes. ...
... The level of external forager loss that can be tolerated is only slightly higher for healthy colonies compared to colonies with Varroa and ABPV. Britton et al. (2021) [99] proposed the first model to study the dynamics of DWV that classified bees as covertly infected (H X ), chronically overtly infected (H Y ), and acutely overtly infected (H Z ), and mites as covert infected (M U ) and overt infected (M V ) based on the infection levels. The model equations for spring, summer, and fall are given by ...
... The level of external forager loss that can be tolerated is only slightly higher for healthy colonies compared to colonies with Varroa and ABPV. Britton et al. (2021) [99] proposed the first model to study the dynamics of DWV that classified bees as covertly infected (H X ), chronically overtly infected (H Y ), and acutely overtly infected (H Z ), and mites as covert infected (M U ) and overt infected (M V ) based on the infection levels. The model equations for spring, summer, and fall are given by ...
Honeybees have an irreplaceable position in agricultural production and the stabilization of natural ecosystems. Unfortunately, honeybee populations have been declining globally. Parasites, diseases, poor nutrition, pesticides, and climate changes contribute greatly to the global crisis of honeybee colony losses. Mathematical models have been used to provide useful insights on potential factors and important processes for improving the survival rate of colonies. In this review, we present various mathematical tractable models from different aspects: 1) simple bee-only models with features such as age segmentation, food collection, and nutrient absorption; 2) models of bees with other species such as parasites and/or pathogens; and 3) models of bees affected by pesticide exposure. We aim to review those mathematical models to emphasize the power of mathematical modeling in helping us understand honeybee population dynamics and its related ecological communities. We also provide a review of computational models such as VARROAPOP and BEEHAVE that describe the bee population dynamics in environments that include factors such as temperature, rainfall, light, distance and quality of food, and their effects on colony growth and survival. In addition, we propose a future outlook on important directions regarding mathematical modeling of honeybees. We particularly encourage collaborations between mathematicians and biologists so that mathematical models could be more useful through validation with experimental data.
Honeybees are important plant pollinators. Unfortunately, there is a growing increase in the loss of honeybee colonies, and this is having a serious economic impact on crop farmers. A major cause of these losses is the parasitic mite Varroadestructor, which is a vector of deformed wing virus (DWV). Some bee species have resistant mechanisms, such as grooming and hygienic behaviours, against Varroa mites. A clear understanding of the effects of these control behaviours on the mites and the viruses they transmit can be important in reducing colony losses. Here, a stochastic model is formulated and analysed to consider the extent to which these control behaviours reduce the probability of an outbreak of DWV in honeybee colonies. Vector and bee-to-bee transmission routes are considered. Using branching process theory, it is shown that without any hygienic or grooming behaviour, a large probability of a DWV outbreak is possible. Also, if bees apply grooming or hygienic behaviour, this can reduce the probability of a virus outbreak, especially in the case of vector transmission, where it can be reduced to zero. Hygienic behaviour is the most significant factor in reducing a DWV outbreak. Thus, bee selection for hygienic behaviour may be important to reduce honeybee colony losses caused by DWV.
The deformed wing virus (DWV) belongs to the genus Iflavirus and the family Iflaviridae within the order Picornavirales. It is an important pathogen of the Western honey bee, Apis mellifera, causing major losses among honey bee colonies in association with the ectoparasitic mite Varroa destructor. Although DWV is one of the best-studied insect viruses, the mechanisms of viral replication and polyprotein processing have been poorly studied in the past. We investigated the processing of the protease-polymerase region at the C-terminus of the polyprotein in more detail using recombinant expression, novel serological reagents, and virus clone mutagenesis. Edman degradation of purified maturated polypeptides uncovered the C- and N-termini of the mature 3C-like (3CL) protease and RNA-dependent RNA polymerase (3DL, RdRp), respectively. Autocatalytic processing of the recombinant DWV 3CL protease occurred at P1 Q2118 and P1′ G2119 (KPQ/GST) as well as P1 Q2393 and P1′ S2394 (HAQ/SPS) cleavage sites. New monoclonal antibodies (Mab) detected the mature 3CL protease with an apparent molecular mass of 32 kDa, mature 3DL with an apparent molecular mass of 55 kDa as well as a dominant 3CDL precursor of 90 kDa in DWV infected honey bee pupae. The observed pattern corresponds well to data obtained via recombinant expression and N-terminal sequencing. Finally, we were able to show that 3CL protease activity and availability of the specific protease cleavage sites are essential for viral replication, protein synthesis, and establishment of infection using our molecular clone of DWV-A.
Living systems, from cells to superorganismic insect colonies, have an organizational boundary between inside and outside and allocate resources to defend it. Whereas the micro-scale dynamics of cell walls can be difficult to study, the adaptive allocation of workers to defense in social-insect colonies is more conspicuous. This is particularly the case for Tetragonisca angustula stingless bees, which combine different defensive mechanisms found across other colonial animals: (1) morphological specialization (distinct soldiers (majors) are produced over weeks); (2) age-based polyethism (young majors transition to guarding tasks over days); and (3) task switching (small workers (minors) replace soldiers within minutes under crisis). To better understand how these timescales of reproduction, development, and behavior integrate to balance defensive demands with other colony needs, we developed a demographic Filippov ODE system to study the effect of these processes on task allocation and colony size. Our results show that colony size peaks at low proportions of majors, but colonies die if minors are too plastic or defensive demands are too high or if there is a high proportion of quickly developing majors. For fast maturation, increasing major production may decrease defenses. This model elucidates the demographic factors constraining collective defense regulation in social insects while also suggesting new explanations for variation in defensive allocation at smaller scales where the mechanisms underlying defensive processes are not easily observable. Moreover, our work helps to establish social insects as model organisms for understanding other systems where the transaction costs for component turnover are nontrivial, as in manufacturing systems and just-in-time supply chains.
Honeybees are the most critical pollinators providing key ecosystem services that underpin crop production and sustainable agriculture. Amidst a backdrop of rapid global change, this eusocial insect encounters a succession of stressors during nesting, foraging, and pollination. Ectoparasitic mites, together with vectored viruses, have been recognized as central biotic threats to honeybee health, while the spread of invasive giant hornets and small hive beetles also increasingly threatens colonies worldwide. Cocktails of agrochemicals, including acaricides used for mite treatment, and other pollutants of the environment have been widely documented to affect bee health in various ways. Additionally, expanding urbanization, climate change, and agricultural intensification often result in the destruction or fragmentation of flower-rich bee habitats. The anthropogenic pressures exerted by beekeeping management practices affect the natural selection and evolution of honeybees, and colony translocations facilitate alien species invasion and disease transmission. In this review, the multiple biotic and abiotic threats and their interactions that potentially undermine bee colony health are discussed, while taking into consideration the sensitivity, large foraging area, dense network among related nestmates, and social behaviors of honeybees.
