A horizon scan of global biological conservation issues for 2022.

We present the results of our 13th annual horizon scan of issues likely to impact on biodiversity conservation. Issues are either novel within the biological conservation sector or could cause a substantial step-change in impact, either globally or regionally. Our global panel of 26 scientists and practitioners identified 15 issues that we believe to represent the highest priorities for tracking and action. Many of the issues we identified, including the impact of satellite megaconstellations and the use of long-distance wireless energy transfer, have both elements of threats and emerging opportunities. A recent state-sponsored application to commence deep-sea mining represents a significant step-change in impact. We hope that this horizon scan will increase research and policy attention on the highlighted issues.

Human-mediated dispersal and disturbance shape the metapopulation dynamics of a long-lived herb.

As anthropogenic impacts on the natural world escalate, there is increasing interest in the role of humans in dispersing seeds. But the consequences of this Human-Mediated Dispersal (HMD) on plant spatial dynamics are little studied. In this paper, we ask how secondary dispersal by HMD affects the dynamics of a natural plant metapopulation. In addition to dispersal between patches, we suggest within-patch processes can be critical. To address this, we assess how variation in local population dynamics, caused by small-scale disturbances, affects metapopulation size. We created an empirically based model with stochastic population dynamics and dispersal among patches, which represented a real-world, cliff-top metapopulation of wild cabbage Brassica oleracea. We collected demographic data from multiple populations by tagging plants over eight years. We assessed seed survival, and establishment and survival of seedlings in intact vegetation vs. small disturbances. We modeled primary dispersal by wind using field data and used experimental data on secondary HMD by hikers. We monitored occupancy patterns over a 14-yr period in the real metapopulation. Disturbance had large effects on local population growth rates, by increasing seedling establishment and survival. This meant that the modeled metapopulation grew in size only when the area disturbed in each patch was above 35%. In these growing metapopulations, although only 0.2% of seeds underwent HMD, this greatly enhanced metapopulation growth rates. Similarly, HMD allowed more colonizations in declining metapopulations under low disturbance, and this slowed the rate of decline. The real metapopulation showed patterns of varying patch occupancy over the survey years, which were related to habitat quality, but also positively to human activity along the cliffs, hinting at beneficial effects of humans. These findings illustrate that realistic changes to dispersal or demography, specifically by humans, can have fundamental effects on the viability of a species at the landscape scale.

Tick-Borne Transmission of Murine Gammaherpesvirus 68.

Herpesviruses are a large group of DNA viruses infecting mainly vertebrates. Murine gammaherpesvirus 68 (MHV68) is often used as a model in studies of the pathogenesis of clinically important human gammaherpesviruses such as Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus. This rodent virus appears to be geographically widespread; however, its natural transmission cycle is unknown. Following detection of MHV68 in field-collected ticks, including isolation of the virus from tick salivary glands and ovaries, we investigated whether MHV68 is a tick-borne virus. Uninfected Ixodes ricinus ticks were shown to acquire the virus by feeding on experimentally infected laboratory mice. The virus survived tick molting, and the molted ticks transmitted the virus to uninfected laboratory mice on which they subsequently fed. MHV68 was isolated from the tick salivary glands, consistent with transmission via tick saliva. The virus survived in ticks without loss of infectivity for at least 120 days, and subsequently was transmitted vertically from one tick generation to the next, surviving more than 500 days. Furthermore, the F1 generation (derived from F0 infected females) transmitted MHV68 to uninfected mice on which they fed, with MHV68 M3 gene transcripts detected in blood, lung, and spleen tissue of mice on which F1 nymphs and F1 adults engorged. These experimental data fulfill the transmission criteria that define an arthropod-borne virus (arbovirus), the largest biological group of viruses. Currently, African swine fever virus (ASFV) is the only DNA virus recognized as an arbovirus. Like ASFV, MHV68 showed evidence of pathogenesis in ticks. Previous studies have reported MHV68 in free-living ticks and in mammals commonly infested with I. ricinus, and neutralizing antibodies to MHV68 have been detected in large mammals (e.g., deer) including humans. Further studies are needed to determine if these reports are the result of tick-borne transmission of MHV68 in nature, and whether humans are at risk of infection.

Research priorities for managing the impacts and dependencies of business upon food, energy, water and the environment.

Delivering access to sufficient food, energy and water resources to ensure human wellbeing is a major concern for governments worldwide. However, it is crucial to account for the 'nexus' of interactions between these natural resources and the consequent implications for human wellbeing. The private sector has a critical role in driving positive change towards more sustainable nexus management and could reap considerable benefits from collaboration with researchers to devise solutions to some of the foremost sustainability challenges of today. Yet opportunities are missed because the private sector is rarely involved in the formulation of deliverable research priorities. We convened senior research scientists and influential business leaders to collaboratively identify the top forty questions that, if answered, would best help companies understand and manage their food-energy-water-environment nexus dependencies and impacts. Codification of the top order nexus themes highlighted research priorities around development of pragmatic yet credible tools that allow businesses to incorporate nexus interactions into their decision-making; demonstration of the business case for more sustainable nexus management; identification of the most effective levers for behaviour change; and understanding incentives or circumstances that allow individuals and businesses to take a leadership stance. Greater investment in the complex but productive relations between the private sector and research community will create deeper and more meaningful collaboration and cooperation.

Root Herbivores Drive Changes to Plant Primary Chemistry, but Root Loss Is Mitigated under Elevated Atmospheric CO2.

Above- and belowground herbivory represents a major challenge to crop productivity and sustainable agriculture worldwide. How this threat from multiple herbivore pests will change under anthropogenic climate change, via altered trophic interactions and plant response traits, is key to understanding future crop resistance to herbivory. In this study, we hypothesized that atmospheric carbon enrichment would increase the amount (biomass) and quality (C:N ratio) of crop plant resources for above- and belowground herbivore species. In a controlled environment facility, we conducted a microcosm experiment using the large raspberry aphid (Amphorophora idaei), the root feeding larvae of the vine weevil (Otiorhynchus sulcatus), and the raspberry (Rubus idaeus) host-plant. There were four herbivore treatments (control, aphid only, weevil only and a combination of both herbivores) and an ambient (aCO2) or elevated (eCO2) CO2 treatment (390 versus 650 ± 50 µmol/mol) assigned to two raspberry cultivars (cv Glen Ample or Glen Clova) varying in resistance to aphid herbivory. Contrary to our predictions, eCO2 did not increase crop biomass or the C:N ratio of the plant tissues, nor affect herbivore abundance either directly or via the host-plant. Root herbivory reduced belowground crop biomass under aCO2 but not eCO2, suggesting that crops could tolerate attack in a CO2 enriched environment. Root herbivory also increased the C:N ratio in leaf tissue at eCO2, potentially due to decreased N uptake indicated by lower N concentrations found in the roots. Root herbivory greatly increased root C concentrations under both CO2 treatments. Our findings confirm that responses of crop biomass and biochemistry to climate change need examining within the context of herbivory, as biotic interactions appear as important as direct effects of eCO2 on crop productivity.

Antagonistic interactions between an invasive alien and a native coccinellid species may promote coexistence.

Despite the capacity of invasive alien species to alter ecosystems, the mechanisms underlying their impact remain only partly understood. Invasive alien predators, for example, can significantly disrupt recipient communities by consuming prey species or acting as an intraguild predator (IGP). Behavioural interactions are key components of interspecific competition between predators, yet these are often overlooked invasion processes. Here, we show how behavioural, non-lethal IGP interactions might facilitate the establishment success of an invading alien species. We experimentally assessed changes in feeding behaviour (prey preference and consumption rate) of native UK coccinellid species (Adalia bipunctata and Coccinella septempunctata), whose populations are, respectively, declining and stable, when exposed to the invasive intraguild predator, Harmonia axyridis. Using a population dynamics model parameterized with these experimental data, we predicted how intraguild predation, accommodating interspecific behavioural interactions, might impact the abundance of the native and invasive alien species over time. When competing for the same aphid resource, the feeding rate of A. bipunctata significantly increased compared to the feeding in isolation, while the feeding rate of H. axyridis significantly decreased. This suggests that despite significant declines in the UK, A. bipunctata is a superior competitor to the intraguild predator H. axyridis. In contrast, the behaviour of non-declining C. septempunctata was unaltered by the presence of H. axyridis. Our experimental data show the differential behavioural plasticity of competing native and invasive alien predators, but do not explain A. bipunctata declines observed in the UK. Using behavioural plasticity as a parameter in a population dynamic model for A. bipunctata and H. axyridis, coexistence is predicted between the native and invasive alien following an initial period of decline in the native species. We demonstrate how empirical and theoretical techniques can be combined to understand better the processes and consequences of alien species invasions for native biodiversity.

A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators.

A summary is provided of recent advances in the natural science evidence base concerning the effects of neonicotinoid insecticides on insect pollinators in a format (a 'restatement') intended to be accessible to informed but not expert policymakers and stakeholders. Important new studies have been published since our recent review of this field (Godfray et al. 2014 Proc. R. Soc. B 281, 20140558. (doi:10.1098/rspb.2014.0558)) and the subject continues to be an area of very active research and high policy relevance.

Bacillus thuringiensis impacts on primary and secondary baculovirus transmission dynamics in Lepidoptera.

Synergistic interactions between entomopathogenic micro-organisms can potentially be exploited to improve biological control of invertebrate pests but empirical data at the population level describing multiple-pathogen transmission dynamics is lacking. We examined how co-inoculation of Bacillus thuringiensis subsp. kurstaki (Btk) and the baculovirus Panolis flammea nucleopolyhedrovirus (PaflNPV) in an experimental field population of Lepidopteran Mamestra brassicae larvae impacted on viral transmission dynamics. We determined how the presence of Btk influenced primary and secondary PaflNPV transmission. When Btk was co-inoculated with PaflNPV, there was increased proportional viral mortality in primary transmission studies compared to plots with virus alone. A delay of up to 4days between applications of Btk and PaflNPV did not impact on primary viral mortality, indicating that a lag between inoculations was unlikely to affect the biocontrol potential of the two pathogens. Viral yields from cadavers in plots with Btk present were significantly lower than those from plots with virus only, and secondary cycling to introduced secondary transmission larvae was significantly reduced. Baculovirus transmission (in terms of the proportion of uninfected larvae in different treatments) was described by a 'refuge' model that allowed for heterogeneity in susceptibility and pathogen exposure. We discuss how transmission may be potentially affected by factors such as host feeding rate, spatial distribution of virus and interactions between pathogens within the insect host. This study improves understanding of the impact of pathogens within host populations and how mixtures of pathogens may be exploited for biocontrol of insect pests.

Why Small Is Beautiful: Wing Colour Is Free from Thermoregulatory Constraint in the Small Lycaenid Butterfly, Polyommatus icarus.

We examined the roles of wing melanisation, weight, and basking posture in thermoregulation in Polyommatus Icarus, a phenotypically variable and protandrous member of the diverse Polyommatinae (Lycaenidae). Under controlled experimental conditions, approximating to marginal environmental conditions for activity in the field (= infrequent flight, long duration basking periods), warming rates are maximised with fully open wings and maximum body temperatures are dependent on weight. Variation in wing melanisation within and between sexes has no effect on warming rates; males and females which differ in melanisation had similar warming rates. Posture also affected cooling rates, consistent with cooling being dependent on convective heat loss. We hypothesise that for this small sized butterfly, melanisation has little or no effect on thermoregulation. This may be a factor contributing to the diversity of wing colours in the Polyommatinae. Because of the importance of size for thermoregulation in this small butterfly, requirements for attaining a suitable size to confer thermal stability in adults may also be a factor influencing larval feeding rates, development time and patterns of voltinism. Our findings indicate that commonly accepted views of the importance of melanisation, posture and size to thermoregulation, developed using medium and large sized butterflies, are not necessarily applicable to small sized butterflies.

Seed bank dynamics govern persistence of Brassica hybrids in crop and natural habitats.

BACKGROUND AND AIMS: Gene flow from crops to their wild relatives has the potential to alter population growth rates and demography of hybrid populations, especially when a new crop has been genetically modified (GM). This study introduces a comprehensive approach to assess this potential for altered population fitness, and uses a combination of demographic data in two habitat types and mathematical (matrix) models that include crop rotations and outcrossing between parental species. METHODS: Full life-cycle demographic rates, including seed bank survival, of non-GM Brassica rapa × B. napus F1 hybrids and their parent species were estimated from experiments in both agricultural and semi-natural habitats. Altered fitness potential was modelled using periodic matrices including crop rotations and outcrossing between parent species. KEY RESULTS: The demographic vital rates (i.e. for major stage transitions) of the hybrid population were intermediate between or lower than both parental species. The population growth rate (λ) of hybrids indicated decreases in both habitat types, and in a semi-natural habitat hybrids became extinct at two sites. Elasticity analyses indicated that seed bank survival was the greatest contributor to λ. In agricultural habitats, hybrid populations were projected to decline, but with persistence times up to 20 years. The seed bank survival rate was the main driver determining persistence. It was found that λ of the hybrids was largely determined by parental seed bank survival and subsequent replenishment of the hybrid population through outcrossing of B. rapa with B. napus. CONCLUSIONS: Hybrid persistence was found to be highly dependent on the seed bank, suggesting that targeting hybrid seed survival could be an important management option in controlling hybrid persistence. For local risk mitigation, an increased focus on the wild parent is suggested. Management actions, such as control of B. rapa, could indirectly reduce hybrid populations by blocking hybrid replenishment.

REVIEW: Towards a risk register for natural capital.

Natural capital is essential for goods and services on which people depend. Yet pressures on the environment mean that natural capital assets are continuing to decline and degrade, putting such benefits at risk. Systematic monitoring of natural assets is a major challenge that could be both unaffordable and unmanageable without a way to focus efforts. Here we introduce a simple approach, based on the commonly used management tool of a risk register, to highlight natural assets whose condition places benefits at risk.We undertake a preliminary assessment using a risk register for natural capital assets in the UK based solely on existing information. The status and trends of natural capital assets are assessed using asset-benefit relationships for ten kinds of benefits (food, fibre (timber), energy, aesthetics, freshwater (quality), recreation, clean air, wildlife, hazard protection and equable climate) across eight broad habitat types in the UK based on three dimensions of natural capital within each of the habitat types (quality, quantity and spatial configuration). We estimate the status and trends of benefits relative to societal targets using existing regulatory limits and policy commitments, and allocate scores of high, medium or low risk to asset-benefit relationships that are both subject to management and of concern.The risk register approach reveals substantial gaps in knowledge about asset-benefit relationships which limit the scope and rigour of the assessment (especially for marine and urban habitats). Nevertheless, we find strong indications that certain assets (in freshwater, mountain, moors and heathland habitats) are at high risk in relation to their ability to sustain certain benefits (especially freshwater, wildlife and climate regulation). Synthesis and applications. With directed data gathering, especially to monitor trends, improve metrics related to asset-benefit relationships, and improve understanding of nonlinearities and thresholds, the natural capital risk register could provide a useful tool. If updated regularly, it could direct monitoring efforts, focus research and protect and manage those natural assets where benefits are at highest risk.

Elevated atmospheric CO2 impairs aphid escape responses to predators and conspecific alarm signals.

Research into the impact of atmospheric change on predator-prey interactions has mainly focused on density dependent responses and trophic linkages. As yet, the chemical ecology underpinning predator-prey interactions has received little attention in environmental change research. Group living animals have evolved behavioral mechanisms to escape predation, including chemical alarm signalling. Chemical alarm signalling between conspecific prey could be susceptible to environmental change if the physiology and behavior of these organisms are affected by changes in dietary quality resulting from environmental change. Using Rubus idaeus plants, we show that elevated concentrations of atmospheric CO2 (eCO2) severely impaired escape responses of the aphid Amphorophora idaei to predation by ladybird larvae (Harmonia axyridis). Escape responses to ladybirds was reduced by >50% after aphids had been reared on plants grown under eCO2. This behavioral response was rapidly induced, occurring within 24 h of being transferred to plants grown at eCO2 and, once induced, persisted even after aphids were transferred to plants grown at ambient CO2. Escape responses were impaired due to reduced sensitivity to aphid alarm pheromone, (E)-ß-farnesene, via an undefined plant-mediated mechanism. Aphid abundance often increases under eCO2, however, reduced efficacy of conspecific signalling may increase aphid vulnerability to predation, highlighting the need to study the chemical ecology of predator-prey interactions under environmental change.

A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators.

There is evidence that in Europe and North America many species of pollinators are in decline, both in abundance and distribution. Although there is a long list of potential causes of this decline, there is concern that neonicotinoid insecticides, in particular through their use as seed treatments are, at least in part, responsible. This paper describes a project that set out to summarize the natural science evidence base relevant to neonicotinoid insecticides and insect pollinators in as policy-neutral terms as possible. A series of evidence statements are listed and categorized according to the nature of the underlying information. The evidence summary forms the appendix to this paper and an annotated bibliography is provided in the electronic supplementary material.

Accounting for habitat when considering climate: has the niche of the Adonis blue butterfly changed in the UK?

The dramatic recovery of three species of grassland specialist butterfly threatened with extinction at their high latitude range limits in the 1980s has been attributed to two factors: increased grazing on calcareous grassland sites and warmer air temperatures. Both result in the warming of soil surface temperatures, favourable to the larvae of these species. We address the influence of both of these factors on the habitat usage of the butterfly Polyommatus bellargus, undergoing recovery at its northern range edge. We test the hypothesis that the larval niche of P. bellargus has become less constrained in the past three decades, whilst controlling for changes in habitat structure. Once habitat change has been accounted for we find no evidence for a broadening of the larval niche of P. bellargus. Further, we show that coincident with the recovery of P. bellargus there have been drastic reductions in average turf height across UK chalk grasslands, but changes in air temperature have been highly variable. We conclude that changes to soil surface temperatures caused by reducing turf heights will have been a more consistent influence than air temperature increases, and so habitat improvements through increased grazing will have been the major driver of recovery in P. bellargus. We consider the need to account for changes in habitat when exploring the impacts of recent climate change on local habitats in thermophilous species, and emphasise the continued importance of habitat management to support such species under variable local climates.

Global climate change and above- belowground insect herbivore interactions.

Predicted changes to the Earth's climate are likely to affect above-belowground interactions. Our understanding is limited, however, by past focus on two-species aboveground interactions mostly ignoring belowground influences. Despite their importance to ecosystem processes, there remains a dearth of empirical evidence showing how climate change will affect above-belowground interactions. The responses of above- and belowground organisms to climate change are likely to differ given the fundamentally different niches they inhabit. Yet there are few studies that address the biological and ecological reactions of belowground herbivores to environmental conditions in current and future climates. Even fewer studies investigate the consequences of climate change for above-belowground interactions between herbivores and other organisms; those that do provide no evidence of a directed response. This paper highlights the importance of considering the belowground fauna when making predictions on the effects of climate change on plant-mediated interspecific interactions.

Reciprocal feeding facilitation between above- and below-ground herbivores.

Interspecific interactions between insect herbivores predominantly involve asymmetric competition. By contrast, facilitation, whereby herbivory by one insect benefits another via induced plant susceptibility, is uncommon. Positive reciprocal interactions between insect herbivores are even rarer. Here, we reveal a novel case of reciprocal feeding facilitation between above-ground aphids (Amphorophora idaei) and root-feeding vine weevil larvae (Otiorhynchus sulcatus), attacking red raspberry (Rubus idaeus). Using two raspberry cultivars with varying resistance to these herbivores, we further demonstrate that feeding facilitation occurred regardless of host plant resistance. This positive reciprocal interaction operates via an, as yet, unreported mechanism. Specifically, the aphid induces compensatory growth, possibly as a prelude to greater resistance/tolerance, whereas the root herbivore causes the plant to abandon this strategy. Both herbivores may ultimately benefit from this facilitative interaction.

Estimating the effects of Cry1F Bt-maize pollen on non-target Lepidoptera using a mathematical model of exposure.

In farmland biodiversity, a potential risk to the larvae of non-target Lepidoptera from genetically modified (GM) Bt-maize expressing insecticidal Cry1 proteins is the ingestion of harmful amounts of pollen deposited on their host plants. A previous mathematical model of exposure quantified this risk for Cry1Ab protein. We extend this model to quantify the risk for sensitive species exposed to pollen containing Cry1F protein from maize event 1507 and to provide recommendations for management to mitigate this risk.A 14-parameter mathematical model integrating small- and large-scale exposure was used to estimate the larval mortality of hypothetical species with a range of sensitivities, and under a range of simulated mitigation measures consisting of non-Bt maize strips of different widths placed around the field edge.The greatest source of variability in estimated mortality was species sensitivity. Before allowance for effects of large-scale exposure, with moderate within-crop host-plant density and with no mitigation, estimated mortality locally was <10% for species of average sensitivity. For the worst-case extreme sensitivity considered, estimated mortality locally was 99·6% with no mitigation, although this estimate was reduced to below 40% with mitigation of 24-m-wide strips of non-Bt maize. For highly sensitive species, a 12-m-wide strip reduced estimated local mortality under 1·5%, when within-crop host-plant density was zero. Allowance for large-scale exposure effects would reduce these estimates of local mortality by a highly variable amount, but typically of the order of 50-fold.Mitigation efficacy depended critically on assumed within-crop host-plant density; if this could be assumed negligible, then the estimated effect of mitigation would reduce local mortality below 1% even for very highly sensitive species.Synthesis and applications. Mitigation measures of risks of Bt-maize to sensitive larvae of non-target lepidopteran species can be effective, but depend on host-plant densities which are in turn affected by weed-management regimes. We discuss the relevance for management of maize events where cry1F is combined (stacked) with a herbicide-tolerance trait. This exemplifies how interactions between biota may occur when different traits are stacked irrespective of interactions between the proteins themselves and highlights the importance of accounting for crop management in the assessment of the ecological impact of GM plants.

Exploring sub-lethal effects of exposure to a nucleopolyhedrovirus in the speckled wood (Pararge aegeria) butterfly.

This study investigated the sub-lethal effects of larval exposure to baculovirus on host life history and wing morphological traits using a model system, the speckled wood butterfly Pararge aegeria (L.) and the virus Autographa californica nucleopolyhedrovirus. Males and females showed similar responses to the viral infection. Infection significantly reduced larval growth rate, whilst an increase in development time allowed the critical mass for pupation to be attained. There was no direct effect of viral infection on the wing morphological traits examined. There was, however, an indirect effect of resisting infection; larvae that took longer to develop had reduced resource investment in adult flight muscle mass.

Feral genetically modified herbicide tolerant oilseed rape from seed import spills: are concerns scientifically justified?

One of the concerns surrounding the import (for food and feed uses or processing) of genetically modified herbicide tolerant (GMHT) oilseed rape is that, through seed spillage, the herbicide tolerance (HT) trait will escape into agricultural or semi-natural habitats, causing environmental or economic problems. Based on these concerns, three EU countries have invoked national safeguard clauses to ban the marketing of specific GMHT oilseed rape events on their territory. However, the scientific basis for the environmental and economic concerns posed by feral GMHT oilseed rape resulting from seed import spills is debatable. While oilseed rape has characteristics such as secondary dormancy and small seed size that enable it to persist and be redistributed in the landscape, the presence of ferals is not in itself an environmental or economic problem. Crucially, feral oilseed rape has not become invasive outside cultivated and ruderal habitats, and HT traits are not likely to result in increased invasiveness. Feral GMHT oilseed rape has the potential to introduce HT traits to volunteer weeds in agricultural fields, but would only be amplified if the herbicides to which HT volunteers are tolerant were used routinely in the field. However, this worst-case scenario is most unlikely, as seed import spills are mostly confined to port areas. Economic concerns revolve around the potential for feral GMHT oilseed rape to contribute to GM admixtures in non-GM crops. Since feral plants derived from cultivation (as distinct from import) occur at too low a frequency to affect the coexistence threshold of 0.9% in the EU, it can be concluded that feral GMHT plants resulting from seed import spills will have little relevance as a potential source of pollen or seed for GM admixture. This paper concludes that feral oilseed rape in Europe should not be routinely managed, and certainly not in semi-natural habitats, as the benefits of such action would not outweigh the negative effects of management.