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The future of biocontrol in the Anthropocene: A review of climate change impacts on biocontrol agents and their hosts

Biological control, the practice of using one species (biocontrol agent) to control the population of another (a host or prey species, hereafter target), can be a successful method to reduce pest species in agricultural and natural systems worldwide. Successful biocontrol agents often share a deep evolutionary history with their targets that results in high target specificity and synchronized phenology. However, with rapidly changing climatic conditions, users of biocontrol agents have questioned how climate change will affect both well-established and more recent biological control relationships. Using a meta-analysis of data collected from a systematic literature review, we evaluated the evidence for the impact of changing temperatures on the efficacy of biocontrol agents and corresponding responses in their targets. Overall, most studies of climate change impacts on biocontrol agents take place in the laboratory and focus on arthropod agents that are parasitoids. Results from our meta-analysis reveal that changes in temperature are projected to impact biocontrol agents and their targets similarly, with no overall significant changes to biocontrol agent or target performance. However, our results also show that temperature responses vary widely across study systems, as illustrated by case studies showing both positive, neutral, and negative effects of temperature on biocontrol agent efficacy, as well as variation in responses across the three core biological control measures of success: survival, reproduction, and efficacy. Our work highlights important knowledge gaps including how climate change will affect both biocontrol agents and their targets simultaneously. Additionally, we find that most current studies of climate impacts examined temperature relationships, predominantly of agricultural biocontrol agents. Increasing the breadth of studies is crucial for understanding the potential for climate change to affect the success of current and future biological control programs.

Ecological Applications

Coastal wetlands in the Anthropocene

We review the functioning and sustainability of coastal marshes and mangroves. Urbanized humans have a 7,000-year-old enduring relationship to coastal wetlands. Wetlands include marshes, salt flats, and saline and freshwater forests. Coastal wetlands occur in all climate zones but are most abundant in deltas. Mangroves are tropical, whereas marshes occur from tropical to boreal areas. Quantification of coastal wetland areas has advanced in recent years but is still insufficiently accurate. Climate change and sea-level rise are predicted to lead to significant wetland losses and other impacts on coastal wetlands and the humans associated with them. Landward migration and coastal retreat are not expected to significantly reduce coastal wetland losses. Nitrogen watershed inputs are unlikely to alter coastal marsh stability because watershed loadings are mostly significantly lower than those in fertilization studies that show decreased belowground biomass and increased decomposition of soil organic matter. Blue carbon is not expected to significantly reduce climate impacts. The high values of ecosystem goods and services of wetlands are expected to be reduced by area losses. Humans have had strong impacts on coastal wetlands in the Holocene, and these impacts are expected to increase in the Anthropocene.

Annual Review of Environment and Resources

The Searsville Lake Site (California, USA) as a candidate Global boundary Stratotype Section and Point for the Anthropocene series

Cores from Searsville Lake within Stanford University’s Jasper Ridge Biological Preserve, California, USA, are examined to identify a potential GSSP for the Anthropocene: core JRBP2018-VC01B (944.5 cm-long) and tightly correlated JRBP2018-VC01A (852.5 cm-long). Spanning from 1900 CE ± 3 years to 2018 CE, a secure chronology resolved to the sub-annual level allows detailed exploration of the Holocene-Anthropocene transition. We identify the primary GSSP marker as first appearance of 239,240 Pu (372–374 cm) in JRBP2018-VC01B and designate the GSSP depth as the distinct boundary between wet and dry season at 366 cm (6 cm above the first sample containing 239,240 Pu) and corresponding to October-December 1948 CE. This is consistent with a lag of 1–2 years between ejection of 239,240 Pu into the atmosphere and deposition. Auxiliary markers include: first appearance of 137 Cs in 1958; late 20th-century decreases in δ 15 N; late 20th-century elevation in SCPs, Hg, Pb, and other heavy metals; and changes in abundance and presence of ostracod, algae, rotifer and protozoan microfossils. Fossil pollen document anthropogenic landscape changes related to logging and agriculture. As part of a major university, the Searsville site has long been used for research and education, serves users locally to internationally, and is protected yet accessible for future studies and communication about the Anthropocene.

California

The San Francisco Estuary, USA as a reference section for an Anthropocene series

A San Francisco Estuary core was analysed at high resolution to assess its component stratigraphic signatures of the Anthropocene in the form of non-native species, Hg, spheroidal carbonaceous particles, δ 13 C org , δ 15 N, radiogenic materials, and heavy metals. Time series analysis of the core using Ti data provides a chronology to depth 167 cm into the 1960s. Below this, to depth 230 cm, the lowermost part of the core may extend to the 1950s or potentially a little earlier. The earliest anthropogenic marker recorded in the core is the excursion in Hg (beginning at 190 cm) which may denote the early 1960s and is the closest stratigraphic marker in the core to the proposed mid-20th century timing for the onset of the Anthropocene. Biostratigraphical signatures of non-native species arriving in the 1970s–1980s are widespread key markers and are significant tools for the correlation of Anthropocene deposits across the estuary. The absence of signals that indicate pre-1950s deposits precludes the use of the core to mark the Holocene–Anthropocene boundary. However, the core provides an important reference section to demonstrate the palaeontological distinctiveness of Anthropocene series deposits.

California

Modeling water quality in the Anthropocene: Directions for the next-generation aquatic ecosystem models

“Everything changes and nothing stands still” (Heraclitus). Here we review three major improvements to freshwater aquatic ecosystem models — and ecological models in general — as water quality scenario analysis tools towards a sustainable future. To tackle the rapid and deeply connected dynamics characteristic of the Anthropocene, we argue for the inclusion of eco-evolutionary, novel ecosystem and social-ecological dynamics. These dynamics arise from adaptive responses in organisms and ecosystems to global environmental change and act at different integration levels and different time scales. We provide reasons and means to incorporate each improvement into aquatic ecosystem models. Throughout this study we refer to Lake Victoria as a microcosm of the evolving novel social-ecological systems of the Anthropocene. The Lake Victoria case clearly shows how interlinked eco-evolutionary, novel ecosystem and social-ecological dynamics are, and demonstrates the need for transdisciplinary research approaches towards global sustainability.

Current Opinion in Environmental Sustainability

Conservation genetics and wild trout: Evolving opportunities to support management

It is increasingly apparent that our planet is undergoing rapid, unprecedented environmental change. These changes are already impacting wild trout populations, leading to declines in occupancy and abundance across increasingly fragmented landscapes. Many changes are projected to intensify in the coming decades, which are likely to be crucial to the future of many wild populations. While there is some uncertainty in exactly how changes will manifest, we can be confident that many populations will need to rapidly adapt to change if they are to persist. The foundation of such rapid change is genetic diversity, and conservation strategies are most likely to be successful when they consider the role of genetics in the outlook for wild trout populations. While not a panacea, rapid advances in the field of conservation genetics allow longstanding questions to be addressed with greater rigor and present new opportunities to support management against a backdrop of accelerating change. Here, we review major advances in conservation genetics as they relate to wild trout and highlight potential opportunities to support conservation in the Anthropocene and key areas of continuing uncertainty.

Conference Paper

Diverse portfolios: Investing in tributaries for restoration of large river fishes in the Anthropocene

Rehabilitation of large Anthropocene rivers requires engagement of diverse stakeholders across a broad range of sociopolitical boundaries. Competing objectives often constrain options for ecological restoration of large rivers whereas fewer competing objectives may exist in a subset of tributaries. Further, tributaries contribute toward building a “portfolio” of river ecosystem assets through physical and biological processes that may present opportunities to enhance the resilience of large river fishes. Our goal is to review roles of tributaries in enhancing mainstem large river fish populations. We present case histories from two greatly altered and distinct large-river tributary systems that highlight how tributaries contribute four portfolio assets to support large-river fish populations: 1) habitat diversity, 2) connectivity, 3) ecological asynchrony, and 4) density-dependent processes. Finally, we identify future research directions to advance our understanding of tributary roles and inform conservation actions. In the Missouri River United States, we focus on conservation efforts for the state endangered lake sturgeon, which inhabits large rivers and tributaries in the Midwest and Eastern United States. In the Colorado River, Grand Canyon United States, we focus on conservation efforts for recovery of the federally threatened humpback chub. In the Missouri River, habitat diversity focused on physical habitats such as substrate for reproduction, and deep-water habitats for refuge, whereas augmenting habitat diversity for Colorado River fishes focused on managing populations in tributaries with minimally impaired thermal and flow regimes. Connectivity enhancements in the Missouri River focused on increasing habitat accessibility that may require removal of physical structures like low-head dams; whereas in the Colorado River, the lack of connectivity may benefit native fishes as the disconnection provides refuge from non-native fish predation. Hydrologic variability among tributaries was present in both systems, likely underscoring ecological asynchrony. These case studies also described density dependent processes that could influence success of restoration actions. Although actions to restore populations varied by river system, these examples show that these four portfolio assets can help guide restoration activities across a diverse range of mainstem rivers and their tributaries. Using these assets as a guide, we suggest these can be transferable to other large river-tributary systems.

Frontiers in Environmental Science

HESS opinions: Beyond the long-term water balance: Evolving Budyko's supply–demand framework for the Anthropocene towards a global synthesis of land-surface fluxes under natural and human-altered watersheds

Global hydroclimatic conditions have been substantially altered over the past century by anthropogenic influences that arise from the warming global climate and from local/regional anthropogenic disturbances. Traditionally, studies have used coupling of multiple models to understand how land-surface water fluxes vary due to changes in global climatic patterns and local land-use changes. We argue that because the basis of the Budyko framework relies on the supply and demand concept, the framework could be effectively adapted and extended to quantify the role of drivers – both changing climate and local human disturbances – in altering the land-surface response across the globe. We review the Budyko framework, along with these potential extensions, with the intent of furthering the applicability of the framework to emerging hydrologic questions. Challenges in extending the Budyko framework over various spatio-temporal scales and the use of global datasets to evaluate the water balance at these various scales are also discussed.

Hydrology and Earth System Sciences

Invasive species control and management: The sea lamprey story

Control of invasive species is a critical component of conservation biology given the catastrophic damage that they can cause to the ecosystems they invade. This is particularly evident with sea lamprey ( Petromyzon marinus ) in the Laurentian Great Lakes. Native to the Atlantic Ocean, the sea lamprey's ability to osmoregulate in fresh water, its wide thermal tolerance, generalist diet, and high fecundity allowed it to rapidly reach pest proportions in the prey-rich Great Lakes once it gained access through shipping canals. The invasion exacerbated declines in Great Lakes fisheries caused by overharvest, culminating in the crash of lake trout ( Salvelinus namaycush ) and other fish populations. In the last 60 years, however, a highly successful sea lamprey control program has reduced sea lamprey to ∼10% of their peak abundance and has been instrumental in enabling the rehabilitation of the Great Lakes ecosystem. In this chapter, we: (1) discuss the likely vectors of the invasion and the physiological attributes of sea lamprey that enabled them to become established in the Great Lakes; (2) review the two cornerstones of the sea lamprey control program—which relies on a combination of pesticides to eradicate multiple generations of larval sea lamprey in their nursey streams, and in-stream barriers to restrict the upstream migration of spawning lamprey—both of which exploit unique physiological vulnerabilities of sea lamprey; (3) describe how sea lamprey control can adversely affect non-target species and how these can be mitigated; (4) show how physiology-based approaches are improving our understanding of the lethal and sublethal effects of sea lamprey on host fishes; and (5) discuss the future of conservation physiology in sea lamprey control. The prime challenge in the next several decades of the Anthropocene will be to further refine the specificity of control tools while maintaining their efficacy, and to adapt to a warming climate and other anthropogenic activities affecting the Great Lakes and their tributaries.

Lake Erie, Lake Huron, Lake Michigan, Lake Ontario

Balancing stability and flexibility in adaptive governance: An analysis of tools available in U.S. environmental law

Adaptive governance must work “on the ground,” that is, it must operate through structures and procedures that the people it governs perceive to be legitimate and fair, as well as incorporating processes and substantive goals that are effective in allowing social-ecological systems (SESs) to adapt to climate change and other impacts. To address the continuing and accelerating alterations that climate change is bringing to SESs, adaptive governance generally will require more flexibility than prior governance institutions have often allowed. However, to function as good governance, adaptive governance must pay real attention to the problem of how to balance this increased need for flexibility with continuing governance stability so that it can foster adaptation to change without being perceived or experienced as perpetually destabilizing, disruptive, and unfair. Flexibility and stability serve different purposes in governance, and a variety of tools exist to strike different balances between them while still preserving the governance institution’s legitimacy among the people governed. After reviewing those purposes and the implications of climate change for environmental governance, we examine psychological insights into the structuring of adaptive governance and the variety of legal tools available to incorporate those insights into adaptive governance regimes. Because the substantive goals of governance systems will differ among specific systems, we do not purport to comment on what the normative or substantive goals of law should be. Instead, we conclude that attention to process and procedure (including participation), as well as increased use of substantive standards (instead of rules), may allow an increased level of substantive flexibility to operate with legitimacy and fairness, providing the requisite levels of psychological, social, and economic stability needed for communities to adapt successfully to the Anthropocene.

Ecology and Society

Sources and sinks of carbon in boreal ecosystems of interior Alaska: a review

Boreal regions store large quantities of carbon but are increasingly vulnerable to carbon loss due to disturbance and climate warming. The boreal region, underlain by discontinuous permafrost, presents a challenging landscape for itemizing current and potential carbon sources and sinks in the boreal soil and vegetation. The roles of fire, forest succession, and the presence (or absence) of permafrost on carbon cycle, vegetation, and hydrologic processes have been the focus of multidisciplinary research in this area for the past 20 years. However, projections of a warming future climate, an increase in fire severity and extent, and the potential degradation of permafrost could lead to major landscape process changes over the next 20 to 50 years. This provides a major challenge for predicting how the interplay between land management activities and impacts of climate warming will affect carbon sources and sinks in Interior Alaska. To assist land managers in adapting and managing for potential changes in the Interior Alaska carbon cycle we developed this review paper incorporating an overview of the climate, ecosystem processes, vegetation types, and soil regimes in Interior Alaska with a focus on ramifications for the carbon cycle. Our objective is to provide a synthesis of the most current carbon storage estimates and measurements to support policy and land management decisions on how to best manage carbon sources and sinks in Interior Alaska. To support this we have surveyed relevant peer reviewed estimates of carbon stocks in aboveground and belowground biomass for Interior Alaska boreal ecosystems. We have also summarized methane and carbon dioxide fluxes from the same ecosystems. These data have been converted into the same units to facilitate comparison across ecosystem compartments. We identify potential changes in the carbon cycle with climate change and human disturbance including how compounding disturbances can affect the boreal system. Finally, we provide recommendations to address the challenges facing land managers in efforts to manage carbon cycle processes. The results of this study can be used for carbon cycle management in other locations within the boreal biome which encompass a broad distribution from 45° to 83° north.

Alaska

Palaeontological signatures of the Anthropocene are distinct from those of previous epochs

The “Great Acceleration” beginning in the mid-20th century provides the causal mechanism of the Anthropocene, which has been proposed as a new epoch of geological time beginning in 1952 CE. Here we identify key parameters and their diagnostic palaeontological signals of the Anthropocene, including the rapid breakdown of discrete biogeographical ranges for marine and terrestrial species, rapid changes to ecologies resulting from climate change and ecological degradation, the spread of exotic foodstuffs beyond their ecological range, and the accumulation of reconfigured forest materials such as medium density fibreboard (MDF) all being symptoms of the Great Acceleration. We show: 1) how Anthropocene successions in North America, South America, Africa, Oceania, Europe, and Asia can be correlated using palaeontological signatures of highly invasive species and changes to ecologies that demonstrate the growing interconnectivity of human systems; 2) how the unique depositional settings of landfills may concentrate the remains of organisms far beyond their geographical range of environmental tolerance; and 3) how a range of settings may preserve a long-lived, unique palaeontological record within post-mid-20th century deposits. Collectively these changes provide a global palaeontological signature that is distinct from all past records of deep-time biotic change, including those of the Holocene.

Earth Science Reviews

Climate impacts on the Gulf of Maine ecosystem: A review of observed and expected changes in 2050 from rising temperatures

The Gulf of Maine has recently experienced its warmest 5-year period (2015–2020) in the instrumental record. This warming was associated with a decline in the signature subarctic zooplankton species, Calanus finmarchicus . The temperature changes have also led to impacts on commercial species such as Atlantic cod ( Gadus morhua ) and American lobster ( Homarus americanus ) and protected species including Atlantic puffins ( Fratercula arctica ) and northern right whales ( Eubalaena glacialis ). The recent period also saw a decline in Atlantic herring ( Clupea harengus ) recruitment and an increase in novel harmful algal species, although these have not been attributed to the recent warming. Here, we use an ensemble of numerical ocean models to characterize expected ocean conditions in the middle of this century. Under the high CO 2 emissions scenario (RCP8.5), the average temperature in the Gulf of Maine is expected to increase 1.1°C to 2.4°C relative to the 1976–2005 average. Surface salinity is expected to decrease, leading to enhanced water column stratification. These physical changes are likely to lead to additional declines in subarctic species including C. finmarchicus , American lobster, and Atlantic cod and an increase in temperate species. The ecosystem changes have already impacted human communities through altered delivery of ecosystem services derived from the marine environment. Continued warming is expected to lead to a loss of heritage, changes in culture, and the necessity for adaptation.

Maine, Massachusetts, New Brunswick, New Hampshire