Stress-induced loss of social resilience in honeybee colonies and its implications on fitness.

Stressors may lead to a shift in the timing of life-history events of species, causing a mismatch with optimal environmental conditions, potentially reducing fitness. In honeybees, the timing of brood rearing and nest emergence in late winter/early spring is critical as colonies need to grow fast after winter to prepare for reproduction. However, the effects of stress on these life-history events in late winter/early spring and the possible consequences are not well understood. Therefore, we tested whether (i) honeybee colonies shift timing of brood rearing and nest emergence as response to stressors, and (ii) if there is a consequent loss of social resilience, reflected in colony fitness (survival, growth and reproduction). We monitored stressed (high load of the parasitic mite Varroa destructor or nutrition restricted) colonies and presumably non-stressed colonies from the beginning of 2020 till spring of 2021. We found that honeybee colonies do not shift the timing of brood rearing and nest emergence in spring as a coping mechanism to stressors. However, we show that there is loss of social resilience in stressed colonies, leading to reduced growth and reproduction. Our study contributes to better understanding the effects of stressors on social resilience in eusocial organisms.

The influence of vertebrate scavengers on leakage of nutrients from carcasses.

The decomposition of carcasses by scavengers and microbial decomposers is an important component of the biochemical cycle that can strongly alter the chemical composition of soils locally. Different scavenger guilds are assumed to have a different influence on the chemical elements that leak into the soil, although this assumption has not been empirically tested. Here, we experimentally determine how different guilds of vertebrate scavengers influence local nutrient dynamics. We performed a field experiment in which we systematically excluded different subsets of vertebrate scavengers from decomposing carcasses of fallow deer (Dama dama), and compared elemental concentrations in the soil beneath and in the vegetation next to the carcasses over time throughout the decomposition process. We used four exclusion treatments: excluding (1) no scavengers, thus allowing them all; (2) wild boar (Sus scrofa); (3) all mammals; and (4) all mammals and birds. We found that fluxes of several elements into the soil showed distinct peaks when all vertebrates were excluded. Especially, trace elements (Cu and Zn) seemed to be influenced by carcass decomposition. However, we found no differences in fluxes between partial exclusion treatments. Thus, vertebrate scavengers indeed reduce leakage of elements from carcasses into the soil, hence influencing local biochemical cycles, but did so independent of which vertebrate scavenger guild had access. Our results suggest that carcass-derived elements are dispersed over larger areas rather than locally leak into the soil when vertebrate scavengers dominate the decomposition process.

On the importance of root traits in seedlings of tropical tree species.

Plant biomass allocation may be optimized to acquire and conserve resources. How trade-offs in the allocation of tropical tree seedlings depend on different stressors remains poorly understood. Here we test whether above- and below-ground traits of tropical tree seedlings could explain observed occurrence along gradients of resources (light, water) and defoliation (fire, herbivory). We grew 24 tree species occurring in five African vegetation types, varying from dry savanna to moist forest, in a glasshouse for 6 months, and measured traits associated with biomass allocation. Classification based on above-ground traits resulted in clusters representing savanna and forest species, with low and high shoot investment, respectively. Classification based on root traits resulted in four clusters representing dry savanna, humid savanna, dry forest and moist forest, characterized by a deep mean rooting depth, root starch investment, high specific root length in deeper soil layers, and high specific root length in the top soil layer, respectively. In conclusion, tree seedlings in this study show root trait syndromes, which vary along gradients of resources and defoliation: seedlings from dry areas invest in deep roots, seedlings from shaded environments optimize shoot investment, and seedlings experiencing frequent defoliation store resources in the roots.

Disturbance regulates the density-body-mass relationship of soil fauna.

Theory on the density-body-mass (DBM) relationship predicts that the density of animal species decreases by the power of -0.75 per unit increase in their body mass, or by the power of -1 when taxa across trophic levels are studied. This relationship is, however, largely debated, as the slope often deviates from the theoretical predictions. Here, we tested the ability of the DBM relationship to reflect changes in the structure of communities subjected to an anthropogenic disturbance. The slope would become less steep if smaller animals were more impacted by the disturbance than the larger ones, whereas the slope would become steeper if larger animals were more affected than the smaller ones. We tested the changes in the DBM relationship by sampling soil fauna, i.e., nematodes, Collembola, and larger arthropods, from a semiarid grassland before and after spraying diesel fuel as disturbance. We applied three different treatments: a control, a light disturbance, and an intense disturbance. We found that the slopes of the DBM relationships before the disturbance were around -1 as predicted by theory. The slope became more positive (i.e., less steep) just after the disturbance, especially after the intense disturbance as smaller fauna suffered the most and early colonizers had larger body mass. Interestingly, we observed that the slopes converged back to -1 by 2 months post-disturbance. Our findings show that the response of soil fauna communities to anthropogenic disturbances could explain the large variation in observed slopes of the DBM relationships. We experimentally demonstrate that an animal community, when disturbed, shows a temporal pattern of DBM relationships ranging from deviations from the predicted slope to convergence to the predicted slope with time. We recommend that deviations in the DBM relationships after disturbances can provide insights in the trajectory of community recovery, and hence could be used for biomonitoring.

Associations between monthly rainfall and mortality in cattle due to East Coast fever, anaplasmosis and babesiosis.

Weather conditions can impact infectious disease transmission, causing mortalities in humans, wild and domestic animals. Although rainfall in dry tropical regions is highly variable over the year, rainfall is thought to play an important role in the transmission of tick-borne diseases. Whether variation in rainfall affects disease-induced mortalities, is, however, poorly understood. Here, we use long-term data on monthly rainfall and Boran cattle mortality (1998-2017) to investigate associations between within-year variation in rainfall and cattle mortalities due to East Coast fever (ECF), anaplasmosis and babesiosis in Laikipia, Kenya, using ARIMAX modelling. Results show a negative correlation between monthly rainfall and cattle mortality for ECF and anaplasmosis, with a lag effect of 2 and 6 months, respectively. There was no association between babesiosis-induced mortalities and monthly rainfall. The results of this study suggest that control of the tick-borne diseases ECF and anaplasmosis to reduce mortalities should be intensified during rainy periods after the respective estimated time lags following dry periods.

Contrasting effects of host species and phylogenetic diversity on the occurrence of HPAI H5N1 in European wild birds.

Studies on the highly pathogenic avian influenza (HPAI) H5N1 suggest that wild bird migration may facilitate its long-distance spread, yet the role of wild bird community composition in its transmission risk remains poorly understood. Furthermore, most studies on the diversity-disease relationship focused on host species diversity without considering hosts' phylogenetic relationships, which may lead to rejecting a species diversity effect when the community has host species that are only distantly related. Here, we explored the influence of waterbird community composition for determining HPAI H5N1 occurrence in wild birds in a continental-scale study across Europe. In particular, we tested the diversity-disease relationship using both host species diversity and host phylogenetic diversity. Our results provide the first demonstration that host community composition-compared with previously identified environmental risk factors-can also effectively explain the spatial pattern of H5N1 occurrence in wild birds. We further show that communities with more higher risk host species and more closely related species have a higher risk of H5N1 outbreaks. Thus, both host species diversity and community phylogenetic structure, in addition to environmental factors, jointly influence H5N1 occurrence. Our work not only extends the current theory on the diversity-disease relationship, but also has important implications for future monitoring of H5N1 and other HPAI subtypes.

On the relationship between fire regime and vegetation structure in the tropics.

We assessed data from 11 experiments examining the effects of the timing and/or frequency of fire on tropical forest and/or savanna vegetation structure over one decade or more. The initial 'control treatment' in many such cases consisted of previously cleared land. This is as opposed to natural vegetation subject to some sort of endogenous fire regime before the imposition of fire treatments. Effects of fire on fractional foliar cover are up to 10-fold greater when clearing pre-treatments are imposed. Moreover, because many of the 'classic' fire trials were initialised with applied management questions in mind, most have also used burning regimes much more frequent and/or severe than those occurring in the absence of human activity. Once these factors are taken into account, our modelling analysis shows that nonanthropogenic fire regimes serve to reduce canopy vegetative cover to a much lower extent than has previously been argued to be the case. These results call into question the notion that fire effects on tropical vegetation can be of a sufficient magnitude to maintain open-type savanna ecosystems under climatic/soil regimes otherwise sufficient to give rise to a more luxurious forest-type vegetation cover.

Declines in moth populations stress the need for conserving dark nights.

Given the global continuous rise, artificial light at night is often considered a driving force behind moth population declines. Although negative effects on individuals have been shown, there is no evidence for effects on population sizes to date. Therefore, we compared population trends of Dutch macromoth fauna over the period 1985-2015 between moth species that differ in phototaxis and adult circadian rhythm. We found that moth species that show positive phototaxis or are nocturnally active have stronger negative population trends than species that are not attracted to light or are diurnal species. Our results indicate that artificial light at night is an important factor in explaining declines in moth populations in regions with high artificial night sky brightness. Our study supports efforts to reduce the impacts of artificial light at night by promoting lamps that do not attract insects and reduce overall levels of illumination in rural areas to reverse declines of moth populations.

Artificial night lighting inhibits feeding in moths.

One major, yet poorly studied, change in the environment is nocturnal light pollution, which strongly alters habitats of nocturnally active species. Artificial night lighting is often considered as driving force behind rapid moth population declines in severely illuminated countries. To understand these declines, the question remains whether artificial light causes only increased mortality or also sublethal effects. We show that moths subjected to artificial night lighting spend less time feeding than moths in darkness, with the shortest time under light conditions rich in short wavelength radiation. These findings provide evidence for sublethal effects contributing to moth population declines. Because effects are strong under various types of light compared with dark conditions, the potential of spectral alterations as a conservation tool may be overestimated. Therefore, restoration and maintenance of darkness in illuminated areas is essential for reversing declines of moth populations.

Does the dilution effect generally occur in animal diseases?

The dilution effect (DE) has been reported in many diseases, but its generality is still highly disputed. Most current criticisms of DE are related to animal diseases. Particularly, some critical studies argued that DE is less likely to occur in complex environments. Here our meta-analyses demonstrated that the magnitude of DE did not differ between animal vs plant diseases. Moreover, DE generally occurs in all three subgroups of animal diseases, namely direct-transmitted diseases, vector-borne diseases and diseases caused by parasites with free-living stages. Our findings serve as an important contribution to understanding the generality of DE.

Scale-dependent bi-trophic interactions in a semi-arid savanna: how herbivores eliminate benefits of nutrient patchiness to plants.

The scale of resource heterogeneity may influence how resources are locally partitioned between co-existing large and small organisms such as trees and grasses in savannas. Scale-related plant responses may, in turn, influence herbivore use of the vegetation. To examine these scale-dependent bi-trophic interactions, we varied fertilizer [(nitrogen (N)/phosphorus (P)/potassium (K)] applications to patches to create different scales of nutrient patchiness (patch size 2 × 2 m, 10 × 10 m, or whole-plot 50 × 50 m) in a large field experiment in intact African savanna. Within-patch fertilizer concentration and the total fertilizer load per plot were independently varied. We found that fertilization increased the leaf N and P concentrations of trees and grasses, resulting in elevated utilization by browsers and grazers. Herbivory off-take was particularly considerable at higher nutrient concentrations. Scale-dependent effects were weak. The net effect of fertilization and herbivory was that plants in fertilized areas tended to grow less and develop smaller rather than larger standing biomass compared to plants growing in areas that remained unfertilized. When all of these effects were considered together at the community (plot) level, herbivory completely eliminated the positive effects of fertilization on the plant community. While this was true for all scales of fertilization, grasses tended to profit more from coarse-grained fertilization and trees from fine-grained fertilization. We conclude that in herbivore-dominated communities, such as the African savanna, nutrient patchiness results in the herbivore community profiting rather more than the plant community, irrespective of the scale of patchiness. At the community level, the allometric scaling theory's prediction of plant-and probably also animal-production does not hold or may even be reversed as a result of complex bi-trophic interactions.

Interaction between Varroa destructor and imidacloprid reduces flight capacity of honeybees.

Current high losses of honeybees seriously threaten crop pollination. Whereas parasite exposure is acknowledged as an important cause of these losses, the role of insecticides is controversial. Parasites and neonicotinoid insecticides reduce homing success of foragers (e.g. by reduced orientation), but it is unknown whether they negatively affect flight capacity. We investigated how exposing colonies to the parasitic mite Varroa destructor and the neonicotinoid insecticide imidacloprid affect flight capacity of foragers. Flight distance, time and speed of foragers were measured in flight mills to assess the relative and interactive effects of high V. destructor load and a field-realistic, chronic sub-lethal dose of imidacloprid. Foragers from colonies exposed to high levels of V. destructor flew shorter distances, with a larger effect when also exposed to imidacloprid. Bee body mass partly explained our results as bees were heavier when exposed to these stressors, possibly due to an earlier onset of foraging. Our findings contribute to understanding of interacting stressors that can explain colony losses. Reduced flight capacity decreases the food-collecting ability of honeybees and may hamper the use of precocious foraging as a coping mechanism during colony (nutritional) stress. Ineffective coping mechanisms may lead to destructive cascading effects and subsequent colony collapse.

Dilution versus facilitation: Impact of connectivity on disease risk in metapopulations.

Epidemiological studies have suggested that increasing connectivity in metapopulations usually facilitates pathogen transmission. However, these studies focusing on single-host systems usually neglect that increasing connectivity can increase species diversity which might reduce pathogen transmission via the 'dilution effect', a hypothesis whose generality is still disputed. On the other hand, studies investigating the generality of the dilution effect were usually conducted without considering habitat structure, which is surprising as species loss is often driven by habitat fragmentation. Using a simple general model to link fragmentation to the dilution effect, we determined the effect of connectivity on disease risk and explored when the dilution effect can be detected. We showed that landscape structure can largely modify the diversity-disease relationship. The net impact of connectivity on disease risk can be either positive or negative, depending on the relative importance of the facilitation effect (through increasing contact rates among patches) versus the dilution effect (via increasing species richness). We also demonstrated that different risk indices (i.e. infection prevalence and abundance of infected hosts) react differently to increasing connectivity and species richness. Our study may contribute to the current debate on the dilution effect, and a better understanding of the impacts of fragmentation on disease risks.

Modeling elephant-mediated cascading effects of water point closure.

Wildlife management to reduce the impact of wildlife on their habitat can be done in several ways, among which removing animals (by either culling or translocation) is most often used. There are, however, alternative ways to control wildlife densities, such as opening or closing water points. The effects of these alternatives are poorly studied. In this paper, we focus on manipulating large herbivores through the closure of water points (WPs). Removal of artificial WPs has been suggested in order to change the distribution of African elephants, which occur in high densities in national parks in Southern Africa and are thought to have a destructive effect on the vegetation. Here, we modeled the long-term effects of different scenarios of WP closure on the spatial distribution of elephants, and consequential effects on the vegetation and other herbivores in Kruger National Park, South Africa. Using a dynamic ecosystem model, SAVANNA, scenarios were evaluated that varied in availability of artificial WPs; levels of natural water; and elephant densities. Our modeling results showed that elephants can indirectly negatively affect the distributions of meso-mixed feeders, meso-browsers, and some meso-grazers under wet conditions. The closure of artificial WPs hardly had any effect during these natural wet conditions. Under dry conditions, the spatial distribution of both elephant bulls and cows changed when the availability of artificial water was severely reduced in the model. These changes in spatial distribution triggered changes in the spatial availability of woody biomass over the simulation period of 80 years, and this led to changes in the rest of the herbivore community, resulting in increased densities of all herbivores, except for giraffe and steenbok, in areas close to rivers. The spatial distributions of elephant bulls and cows showed to be less affected by the closure of WPs than most of the other herbivore species. Our study contributes to ecologically informed decisions in wildlife management. The results from this modeling exercise imply that long-term effects of this intervention strategy should always be investigated at an ecosystem scale.

Relative growth rate variation of evergreen and deciduous savanna tree species is driven by different traits.

BACKGROUND AND AIMS: Plant relative growth rate (RGR) depends on biomass allocation to leaves (leaf mass fraction, LMF), efficient construction of leaf surface area (specific leaf area, SLA) and biomass growth per unit leaf area (net assimilation rate, NAR). Functional groups of species may differ in any of these traits, potentially resulting in (1) differences in mean RGR of groups, and (2) differences in the traits driving RGR variation within each group. We tested these predictions by comparing deciduous and evergreen savanna trees. METHODS: RGR, changes to biomass allocation and leaf morphology, and root non-structural carbohydrate reserves were evaluated for juveniles of 51 savanna species (34 deciduous, 17 evergreen) grown in a common garden experiment. It was anticipated that drivers of RGR would differ between leaf habit groups because deciduous species have to allocate carbohydrates to storage in roots to be able to flush leaves again, which directly compromises their LMF, whereas evergreen species are not subject to this constraint. KEY RESULTS: Evergreen species had greater LMF and RGR than deciduous species. Among deciduous species LMF explained 27 % of RGR variation (SLA 34 % and NAR 29 %), whereas among evergreen species LMF explained between 2 and 17 % of RGR variation (SLA 32-35 % and NAR 38-62 %). RGR and LMF were (negatively) related to carbohydrate storage only among deciduous species. CONCLUSIONS: Trade-offs between investment in carbohydrate reserves and growth occurred only among deciduous species, leading to differences in relative contribution made by the underlying components of RGR between the leaf habit groups. The results suggest that differences in drivers of RGR occur among savanna species because these have different selected strategies for coping with fire disturbance in savannas. It is expected that variation in the drivers of RGR will be found in other functional types that respond differently to particular disturbances.

Tree species from different functional groups respond differently to environmental changes during establishment.

Savanna plant communities change considerably across time and space. The processes driving savanna plant species diversity, coexistence and turnover along environmental gradients are still unclear. Understanding how species respond differently to varying environmental conditions during the seedling stage, a critical stage for plant population dynamics, is needed to explain the current composition of plant communities and to enable us to predict their responses to future environmental changes. Here we investigate whether seedling response to changes in resource availability, and to competition with grass, varied between two functional groups of African savanna trees: species with small leaves, spines and N-fixing associations (fine-leaved species), and species with broad leaves, no spines, and lacking N-fixing associations (broad-leaved species). We show that while tree species were strongly suppressed by grass, the effect of resource availability on seedling performance varied considerably between the two functional groups. Nutrient inputs increased stem length only of broad-leaved species and only under an even watering treatment. Low light conditions benefited mostly broad-leaved species' growth. Savannas are susceptible to ongoing global environment changes. Our results suggest that an increase in woody cover is only likely to occur in savannas if grass cover is strongly suppressed (e.g. by fire or overgrazing). However, if woody cover does increase, broad-leaved species will benefit most from the resulting shaded environments, potentially leading to an expansion of the distribution of these species. Eutrophication and changes in rainfall patterns may also affect the balance between fine- and broad-leaved species.

Influence of tree cover on carcass detection and consumption by facultative vertebrate scavengers.

Scavenging mammals and vultures can exploit and deplete carcasses much faster than other birds and invertebrates. Vultures are strongly influenced by habitat type, e.g. tree cover, since they rely on their eyesight to detect carcasses. It remains unclear whether and how facultative scavengers - both other birds and mammals - are influenced by tree cover and how that affect carcass decomposition time, which in turn affects biodiversity and ecological processes, including the cycle of energy and nutrients. We studied whether the carcass detection and consumption, hence carcass decomposition speed, by facultative avian and mammalian scavengers varies with tree cover in areas without vultures. Fresh mammal carcasses were placed in different landscapes across the Netherlands at locations that widely varied in tree cover. Camera traps were used to record carcass exploitation by facultative avian and mammalian scavengers and to estimate carcass decomposition time. We found that carcass detection and consumption by birds, wild boar, and other mammals varied between locations. Carcass decomposition speed indeed increased with carcass detection and exploitation by mammals, especially by wild boar. However, this variation was not related to tree cover. We conclude that tree cover is not a major determinant of carcass exploitation by facultative scavengers in areas without obligate scavengers and large carnivores.

Dilution effect in bovine tuberculosis: risk factors for regional disease occurrence in Africa.

Changes in host diversity have been postulated to influence the risk of infectious diseases, including both dilution and amplification effects. The dilution effect refers to a negative relationship between biodiversity and disease risk, whereas the amplification effect occurs when biodiversity increases disease risk. We tested these effects with an influential disease, bovine tuberculosis (BTB), which is widespread in many countries, causing severe economic losses. Based on the BTB outbreak data in cattle from 2005 to 2010, we also tested, using generalized linear mixed models, which other factors were associated with the regional BTB presence in cattle in Africa. The interdependencies of predictors and their correlations with BTB presence were examined using path analysis. Our results suggested a dilution effect, where increased mammal species richness was associated with reduced probability of BTB presence after adjustment for cattle density. In addition, our results also suggested that areas with BTB infection in the preceding year, higher cattle density and larger percentage of area occupied by African buffalo were more likely to report BTB outbreaks. Climatic variables only indirectly influenced the risk of BTB presence through their effects on cattle density and wildlife distribution. Since most studies investigating the role of wildlife species on BTB transmission only involve single-species analysis, more efforts are needed to better understand the effect of the structure of wildlife communities on BTB dynamics.

Deciduous and evergreen trees differ in juvenile biomass allometries because of differences in allocation to root storage.

BACKGROUND AND AIMS: Biomass partitioning for resource conservation might affect plant allometry, accounting for a substantial amount of unexplained variation in existing plant allometry models. One means of resource conservation is through direct allocation to storage in particular organs. In this study, storage allocation and biomass allometry of deciduous and evergreen tree species from seasonal environments were considered. It was expected that deciduous species would have greater allocation to storage in roots to support leaf regrowth in subsequent growing seasons, and consequently have lower scaling exponents for leaf to root and stem to root partitioning, than evergreen species. It was further expected that changes to root carbohydrate storage and biomass allometry under different soil nutrient supply conditions would be greater for deciduous species than for evergreen species. METHODS: Root carbohydrate storage and organ biomass allometries were compared for juveniles of 20 savanna tree species of different leaf habit (nine evergreen, 11 deciduous) grown in two nutrient treatments for periods of 5 and 20 weeks (total dry mass of individual plants ranged from 0·003 to 258·724 g). KEY RESULTS: Deciduous species had greater root non-structural carbohydrate than evergreen species, and lower scaling exponents for leaf to root and stem to root partitioning than evergreen species. Across species, leaf to stem scaling was positively related, and stem to root scaling was negatively related to root carbohydrate concentration. Under lower nutrient supply, trees displayed increased partitioning to non-structural carbohydrate, and to roots and leaves over stems with increasing plant size, but this change did not differ between leaf habits. CONCLUSIONS: Substantial unexplained variation in biomass allometry of woody species may be related to selection for resource conservation against environmental stresses, such as resource seasonality. Further differences in plant allometry could arise due to selection for different types of biomass allocation in response to different environmental stressors (e.g. fire vs. herbivory).