Tracking flight activity of potato leafhopper (Hemiptera: Cicadellidae) with the Midwest Suction Trap Network.

Potato leafhopper (PLH), Empoasca fabae Harris (Hemiptera: Cicadellidae), is an economic pest of a variety of crops that migrates between overwintering sites in the southern United States and northern breeding grounds. Since 2005, the Midwest Suction Trap Network (STN) has monitored the magnitude and timing of aerially dispersing aphids' activity, but the potential of the network to monitor other taxa is only beginning to be explored. Here, we use the Midwest STN to examine how the magnitude and timing of PLH activity vary with weather, cropland cover, and time of year. We found that weekly PLH activity increased early in the season (May-June) with increasing degree day accumulation and decreased mid-season (July-August) with increasing occurrence of rain. The first detections occurred earlier in southern latitudes, while the last detections occurred sooner, when there was more surrounding potato land cover, and later over time between 2018 and 2021 and in southern latitudes. PLH activity was thus longer in duration in southern latitudes and has continued to extend later into the year overall. Resolving uncertainty about how well the Midwest STN captures migratory activity and how closely suction trap detections reflect local population densities in crop fields remain important research priorities before the potential of the Midwest STN for PLH monitoring can be realized. Still, observed patterns suggest that PLH could increase in economic importance as insects disperse over larger portions of the growing season in the warming, agriculturally productive US Midwest and that the STN can become a useful tool to monitor these changes.

Temporal and spatial dynamics of the emerald ash borer invasion in Connecticut as shown by the native digging wasp Cerceris fumipennis (Hymenoptera: Crabronidae).

Detecting and monitoring populations of the invasive emerald ash borer (EAB) is crucial to successful management of the pest and evaluation of its ecological impacts. However, the beetle's cryptic habit makes accurate monitoring costly and time-consuming. Biosurveillance takes advantage of the foraging effort of a predatory wasp Cerceris fumipennis (Hymenoptera: Crabronidae). This native, solitary, ground-nesting hunting wasp hunts adult buprestid beetles to provision its brood cells. By intercepting the hunting wasps, we can learn which species of buprestids are in the surrounding forest. The resulting data provides information on the presence and relative abundance of invasive buprestids like EAB which can supplement other monitoring efforts. In this paper we share results of ten years of biosurveillance surveys of the EAB in Connecticut. Among 112 sites, we observed EAB populations; from first detection, through the population peak and then through to the population crash, matching patterns observed in other regions of the United States. We also observed the spread of the EAB relative abundance as it moved through the state following an invasion front starting in New Haven, Co. The average time from first detection to population crash was nine years. On average, populations peaked three years after first detection, and remained at peak levels for three to four years. Population decline was gradual and took another three to four years. Notably, no evidence of a second introduction to Connecticut was seen with proportional abundance increasing over time after expanding outward from the introduction point. These results corroborate other traditional monitoring efforts in the eastern U.S. and provide independent validation of predicted population dynamics in ash stands.

A way forward for design and analysis of neuroimaging studies of memory consolidation.

Several novel ideas and suggestions were made in response to our discussion paper (Tallman et al., this issue). Careful consideration of the content and context of memory while accounting for the neuroanatomy and functional specialization of the hippocampus may reveal more consistent patterns in fMRI studies of memory consolidation. Below we address these ideas as well as issues that arise when interpreting the fMRI signal in memory consolidation studies. In addition, we describe new analyses suggested by the commentators that clarify our findings with respect to current theories.

Human brain activity and functional connectivity as memories age from one hour to one month.

Theories of memory consolidation suggest the role of brain regions and connectivity between brain regions change as memories age. Human lesion studies indicate memories become hippocampus-independent over years, whereas animal studies suggest this process occurs across relatively short intervals, from days to weeks. Human neuroimaging studies suggest that changes in hippocampal and cortical activity and connectivity can be detected over these short intervals, but many of these studies examined only two time periods. We examined memory and fMRI activity for photos of indoor and outdoor scenes across four time periods to examine these neural changes more carefully. Participants (N = 21) studied scenes 1 hour, 1 day, 1 week, or 1 month before scanning. During scanning, participants viewed scenes, made old/new recognition memory judgments, and gave confidence ratings. Memory accuracy, confidence ratings, and response times changed with memory age. Brain activity in a widespread cortical network either increased or decreased with memory age, whereas hippocampal activity was not related to memory age. These findings were almost identical when effects of behavioral changes across time periods were minimized. Functional connectivity of the ventromedial prefrontal cortex with the posterior parietal cortex increased with memory age. By contrast, functional connectivity of the hippocampus with the parahippocampal cortex and fusiform gyrus decreased with memory age. In sum, we detected changes in cortical activity and changes in hippocampal and cortical connectivity with memory age across short intervals. These findings provide support for the predictions of systems consolidation and suggest that these changes begin soon after memories are formed.

Responses of pea plants to multiple antagonists are mediated by order of attack and phytohormone crosstalk.

Plants are often attacked by multiple antagonists and traits of the attacking organisms and their order of arrival onto hosts may affect plant defences. However, few studies have assessed how multiple antagonists, and varying attack order, affect plant defence or nutrition. To address this, we assessed defensive and nutritional responses of Pisum sativum plants after attack by a vector herbivore (Acrythosiphon pisum), a nonvector herbivore (Sitona lineatus), and a pathogen (Pea enation mosaic virus, PEMV). We show viruliferous A. pisum induced several antipathogen plant defence signals, but these defences were inhibited by S. lineatus feeding on peas infected with PEMV. In contrast, S. lineatus feeding induced antiherbivore defence signals, and these plant defences were enhanced by PEMV. Sitona lineatus also increased abundance of plant amino acids, but only when they attacked after viruliferous A. pisum. Our results suggest that diverse communities of biotic antagonists alter defence and nutritional traits of plants through complex pathways that depend on the identity of attackers and their order of arrival onto hosts. Moreover, we show interactions among a group of biotic stressors can vary along a spectrum from antagonism to enhancement/synergism based on the identity and order of attackers, and these interactions are mediated by a multitude of phytohormone pathways.

Vector-borne plant pathogens modify top-down and bottom-up effects on insect herbivores.

Ecological theory predicts that host-plant traits affect herbivore population growth rates, which in turn modulates predator-prey interactions. However, while vector-borne plant pathogens often alter traits of both host plants and vectors, a few studies have assessed how pathogens may act as interaction modifiers within tri-trophic food webs. By applying a food web motif framework, we assessed how a vector-borne plant pathogen (Pea-enation mosaic virus, PEMV) modified both bottom-up (plant-herbivore) and top-down (predator-prey) interactions. Specifically, we assessed trophic interactions with PEMV-infectious Acyrthosiphon pisum (pea aphid) vectors compared to non-infectious aphids in a factorial experiment that manipulated predator and plant communities. We show that PEMV altered bi-trophic relationships, whereby on certain plant species, PEMV reduced vector performance but also increased their susceptibility to predators. However, on other plant species, PEMV weakened top-down control or increased vector performance. Our results suggest that vector-borne plant pathogens are important interaction modifiers for plant-herbivore-predator dynamics: host-plant response to viruses can decrease herbivore abundance by reducing herbivore performance, but also increase herbivore abundance by weakening top-down control. Broadly speaking, trophic interactions that regulate herbivore outbreaks appear to be modified for herbivores actively transmitting viruses to host plants. Consequently, management and monitoring of outbreaking herbivores should consider the infection status of focal populations.

Effects of Agronomic Practices on Lygus spp. (Hemiptera: Miridae) Population Dynamics in Quinoa.

Crop diversification often promotes farm sustainability. However, proper management of newly introduced crops is difficult when pests are unknown. Characterizing herbivore dynamics on new crops, and how they respond to agronomic factors, is crucial for integrated pest management. Here we explored factors affecting Lygus spp. (Hemiptera: Miridae) herbivores in quinoa crops of Washington State. Quinoa is a newly introduced crop for North America that has multiple varieties and a range of agronomic practices used for cultivation. Through arthropod surveys and discussions with growers, we determined that Lygus spp. was the most abundant insect herbivore and likely contributed to low quinoa yields in previous seasons. We assessed how different varieties (Pison and QQ74), irrigation regimes (present and not), and planting methods (direct-seeded and transplanted) affected Lygus population dynamics. Lygus phenology was correlated with timing of quinoa seed-set in July and August, corresponding to a period when quinoa is most susceptible to Lygus. Both irrigation and planting manipulations had significant effects on Lygus abundance. Irrigation reduced Lygus abundance compared with nonirrigated plots in 2018. Planting method had a significant effect on Lygus populations in both 2017 and 2018, but effects differed among years. Variety had a significant effect on Lygus abundance, but only in nonirrigated plots. Overall, our study shows that Lygus is a common insect herbivore in quinoa, and careful selection of variety, planting method, and irrigation regime may be key components of effective control in seasons where Lygus abundance is high.

Ants of the Palouse Prairie: diversity and species composition in an endangered grassland.

Grasslands are globally imperilled ecosystems due to widespread conversion to agriculture and there is a concerted effort to catalogue arthropod diversity in grasslands to guide conservation decisions. The Palouse Prairie is one such endangered grassland; a mid-elevation habitat found in Washington and Idaho, United States. Ants (Formicidae) are useful indicators of biodiversity and historical ecological disturbance, but there has been no structured sampling of ants in the Palouse Prairie. To fill this gap, we employed a rapid inventory sampling approach using pitfall traps to capture peak ant activity in five habitat fragments. We complemented our survey with a systemic review of field studies for the ant species found in Palouse Prairie. Our field inventory yielded 17 ant species across 10 genera and our models estimate the total ant species pool to be 27. The highest ant diversity was found in an actively-managed ecological trust in Latah County, Idaho, suggesting that restoration efforts may increase biodiversity. We also report two rarely-collected ants in the Pacific Northwest and a microgyne that may represent an undescribed species related to Brachymyrmex depilis. Our score-counting review revealed that grassland ants in Palouse Prairie have rarely been studied previously and that more ant surveys in temperate grasslands have lagged behind sampling efforts of other global biomes.

A role for medial entorhinal cortex in spatial and nonspatial forms of memory in rats.

Many studies have focused on the role of the medial entorhinal cortex (MEC) in spatial memory and spatial processing. However, more recently, studies have suggested that the functions of the MEC may extend beyond the spatial domain and into the temporal aspects of memory processing. The current study examined the effect of MEC lesions on spatial and nonspatial tasks that require rats to learn and remember information about location or stimulus-stimulus associations across short temporal gaps. MEC- and sham-lesioned male rats were tested on a watermaze delayed match to position (DMP) task and trace fear conditioning (TFC). Rats with MEC lesions were impaired at remembering the platform location after both the shortest (1 min) and the longest (6 h) delays on the DMP task, never performing as precisely as sham rats under the easiest condition and performing poorly at the longest delay. On the TFC task, although MEC-lesioned rats were not impaired at remembering the conditioning context, they showed reduced freezing in response to the previously associated tone. These findings suggest that the MEC plays a role in bridging temporal delays during learning and memory that extend beyond its established role in spatial memory processing.

Insect alarm pheromones in response to predators: Ecological trade-offs and molecular mechanisms.

Insect alarm pheromones are chemical substances that are synthesized and released in response to predators to reduce predation risk. Alarm pheromones can also be perceived by predators, who take advantage of alarm cues to locate prey. While selection favors evolution of alarm pheromone signals that are not easily detectable by predators, predator evolution selects for better prey detection ability. Here, we review the diversity of alarm signals, and consider the behavioral and ecological conditions under which they have evolved. We show that components of alarm pheromones are similar across many insects, although aphids exhibit different behavioral responses to alarm cues compared to social insects. The effects of alarm pheromones on prey behavior depend on factors such as the concentration of pheromones and the density of conspecifics. We also discuss the molecular mechanisms of alarm pheromone perception underlying the evolutionary arms race between predators and prey, and the function of olfactory proteins and receptors in particular. Our review provides a novel synthesis of the diversity and function of insect alarm pheromones, while suggesting avenues that might better allow researchers to exploit population-level responses to alarm signaling for the sustainable management of pests and vector-borne pathogens.

Dietary specialization is conditionally associated with increased ant predation risk in a temperate forest caterpillar community.

The enemy-free space hypothesis (EFSH) contends that generalist predators select for dietary specialization in insect herbivores. At a community level, the EFSH predicts that dietary specialization reduces predation risk, and this pattern has been found in several studies addressing the impact of individual predator taxa or guilds. However, predation at a community level is also subject to combinatorial effects of multiple-predator types, raising the question of how so-called multiple-predator effects relate to dietary specialization in insect herbivores. Here, we test the EFSH with a field experiment quantifying ant predation risk to insect herbivores (caterpillars) with and without the combined predation effects of birds. Assessing a community of 20 caterpillar species, we use model selection in a phylogenetic comparative framework to identify the caterpillar traits that best predict the risk of ant predation. A caterpillar species' abundance, dietary specialization, and behavioral defenses were important predictors of its ant predation risk. Abundant caterpillar species had increased risk of ant predation irrespective of bird predation. Caterpillar species with broad diet breadth and behavioral responsiveness to attack had reduced ant predation risk, but these ant effects only occurred when birds also had access to the caterpillar community. These findings suggest that ant predation of caterpillar species is density- or frequency-dependent, that ants and birds may impose countervailing selection on dietary specialization within the same herbivore community, and that contingent effects of multiple predators may generate behaviorally mediated life-history trade-offs associated with herbivore diet breadth.

Plant-mediated interactions between a vector and a non-vector herbivore promote the spread of a plant virus.

Herbivores that transmit plant pathogens often share hosts with non-vector herbivores. These co-occurring herbivores can affect vector fitness and behaviour through competition and by altering host plant quality. However, few studies have examined how such interactions may both directly and indirectly influence the spread of a plant pathogen. Here, we conducted field and greenhouse trials to assess whether a defoliating herbivore (Sitona lineatus) mediated the spread of a plant pathogen, Pea enation mosaic virus (PEMV), by affecting the fitness and behaviour of Acrythosiphon pisum, the PEMV vector. We observed higher rates of PEMV spread when infectious A. pisum individuals shared hosts with S. lineatus individuals. Using structural equation models, we showed that herbivory from S. lineatus increased A. pisum fitness, which stimulated vector movement and PEMV spread. Moreover, plant susceptibility to PEMV was indirectly enhanced by S. lineatus, which displaced A. pisum individuals to the most susceptible parts of the plant. Subsequent analyses of plant defence genes revealed considerable differences in plant phytohormones associated with anti-herbivore and anti-pathogen defence when S. lineatus was present. Given that vectors interact with non-vector herbivores in natural and managed ecosystems, characterizing how such interactions affect pathogens would greatly enhance our understanding of disease ecology.

Invasive Japanese Barberry, Berberis thunbergii (Ranunculales: Berberidaceae) Is Associated With Simplified Branch-Dwelling and Leaf-Litter Arthropod Communities in a New York Forest.

Arthropod food webs can be indirectly impacted by woody plant invasions, with cascading consequences for higher trophic levels. There are multiple bottom-up pathways by which invasive plants can alter food webs: above-ground interactions based on plant-herbivore associations and below-ground at the interface of leaf-litter and soil food webs. We compared arthropod community composition in these two food web dimensions in a New York forest that has been heavily invaded by nonnative Japanese barberry. Using two sampling protocols, we compared arthropod community composition on Japanese barberry shrubs to multiple species of native host shrubs and then compared leaf-litter arthropod assemblages between forest patches with exceptionally high Japanese barberry densities and those with relatively little to no Japanese barberry present. Fitting with trends in other woody shrub invasions, arthropod species richness was significantly lower in the leaf litter around Japanese barberry and on Japanese barberry plants themselves. Although overall arthropod abundance was also significantly lower on and in the leaf litter around Japanese barberry than on and around native shrubs, total biomass did not differ due to the taxa associated with Japanese barberry tending to be larger-bodied. We observed a dramatic reduction in predatory arthropods in response to both bottom-up pathways, particularly among ants and spiders. Our results show that Japanese barberry-invaded habitats may be experiencing trophic downgrading as result of lower numbers of generalist predators like spiders and ants, which may have rippling effects up the food web to insectivorous animals and their predators.

Tri-trophic interactions mediate the spread of a vector-borne plant pathogen.

Many insect herbivores are vectors that transmit plant pathogens as they forage. Within food webs, vectors interact with a range of host plants, other herbivores, and predators. Yet, few studies have examined how tri-trophic interactions involving vectors affect the spread of pathogens. Here we assessed effects of food web structure on aphid vectors and the prevalence of an aphid-borne persistent pathogen (Pea enation mosaic virus, PEMV) in pea plants. We experimentally manipulated ladybird predators, alternative host plants, and non-vector herbivores and assessed responses of pea aphids and PEMV using structural equation models. We show that variation in bottom-up, top-down, and horizontal interactions mediated PEMV prevalence. Predators reduced PEMV prevalence by consuming aphids, but an alternative host plant (vetch) had the opposite effect by promoting aphid movement and abundance. Non-vector herbivores (pea leaf weevil) increased PEMV susceptibility in peas. In turn, weevils offset the positive effects of predators on PEMV, but increased the negative effects of vetch. Our results show that tri-trophic interactions within insect and plant food webs can mediate vector biology with synergistic and opposing effects on pathogens. Continuing to assess how community-wide interactions affect vectors will aid in our understanding of vector-borne pathosystems.

Cognitive and Microbiome Impacts of Experimental Ancylostoma ceylanicum Hookworm Infections in Hamsters.

Hookworms are one of the most prevalent and important parasites, infecting ~500 million people worldwide. Hookworm disease is among the leading causes of iron-deficiency anemia in the developing world and is associated with significant growth stunting and malnutrition. In humans, hookworms appear to impair memory and other forms of cognition, although definitive data are hard to come by. Here we study the impact of a human hookworm parasite, Ancylostoma ceylanicum, on cognition in hamsters in a controlled laboratory setting. We developed tests that measure long-term memory in hamsters. We find that hookworm-infected hamsters were fully capable of detecting a novel object. However, hookworm-infected hamsters were impaired in detecting a displaced object. Defects could be discerned at even at low levels of infection, whereas at higher levels of infection, hamsters were statistically unable to distinguish between displaced and non-displaced objects. These spatial memory deficiencies could not be attributed to defects in infected hamster mobility or to lack of interest. We also found that hookworm infection resulted in reproducible reductions in diversity and changes in specific taxanomic groups in the hamster gut microbiome. These data demonstrate that human hookworm infection in a laboratory mammal results in a specific, rapid, acute, and measurable deficit in spatial memory, and we speculate that gut alterations could play some role in these cognitive deficits. Our findings highlight the importance of hookworm elimination and suggest that finer tuned spatial memory studies be carried out in humans.

Time Cells in the Hippocampus Are Neither Dependent on Medial Entorhinal Cortex Inputs nor Necessary for Spatial Working Memory.

A key function of the hippocampus and entorhinal cortex is to bridge events that are discontinuous in time, and it has been proposed that medial entorhinal cortex (mEC) supports memory retention by sustaining the sequential activity of hippocampal time cells. Therefore, we recorded hippocampal neuronal activity during spatial working memory and asked whether time cells depend on mEC inputs. Working memory was impaired in rats with mEC lesions, but the occurrence of time cells and of trajectory-coding cells in the stem did not differ from controls. Rather, the main effect of mEC lesions was an extensive spatial coding deficit of CA1 cells, which included inconsistency over time and reduced firing differences between positions on the maze. Therefore, mEC is critical for providing stable and distinct spatial information to hippocampus, while working memory (WM) maintenance is likely supported either by local synaptic plasticity in hippocampus or by activity patterns elsewhere in the brain.

Recent and remote retrograde memory deficit in rats with medial entorhinal cortex lesions.

The hippocampus is critically involved in the acquisition and retrieval of spatial memories. Even though some memories become independent of the hippocampus over time, expression of spatial memories have consistently been found to permanently depend on the hippocampus. Recent studies have focused on the adjacent medial entorhinal cortex (MEC), as it provides major projections to the hippocampus. These studies have shown that lesions of the MEC disrupt spatial processing in the hippocampus and impair spatial memory acquisition on the watermaze task. MEC lesions acquired after learning the watermaze task also disrupt recently acquired spatial memories. However, the effect of MEC lesions on remotely acquired memories is unknown. The current study examined the effect of MEC lesions on recent and remote memory retrieval using three hippocampus-dependent tasks: the watermaze, trace fear conditioning, and novel object recognition. MEC lesions caused impaired retrieval of recently and remotely acquired memory for the watermaze. Rats with MEC lesions also showed impaired fear memory when exposed to the previously conditioned context or the associated tone, and this reduction was seen both when the lesion occurred soon after trace fear condition and when it occurred a month after conditioning. In contrast, MEC lesions did not disrupt novel object recognition. These findings indicate that even with an intact hippocampus, rats with MEC lesions cannot retrieve recent or remote spatial memories. In addition, the involvement of the MEC in memory extends beyond is role in navigation and place memory.

A History and Overview of the Behavioral Neuroscience of Learning and Memory.

Here, I provide a basic history of important milestones in the development of theories for how the brain accomplishes the phenomenon of learning and memory. Included are the ideas of Plato, René Descartes, Théodule Ribot, William James, Ivan Pavlov, John Watson, Karl Lashley, and others. The modern era of learning and memory research begins with the description of H.M. by Brenda Milner and the gradual discovery that the brain contains multiple learning and memory systems that are supported by anatomically discrete brain structures. Finally, a brief overview is provided for the chapters that are included in current topics in Behavioral Neuroscience-Learning and Memory.

Current Topics Regarding the Function of the Medial Temporal Lobe Memory System.

The first clear insight that the medial temporal lobe of the human brain was in fact a system of anatomically connected structures that were organized into a memory system came in 1957 from the observations by Brenda Milner of the noted amnesic patient H.M. Subsequent work in humans, monkeys, and rodents has identified all of the components of the medial temporal lobe (MTL) that formed the memory system. Currently, work is ongoing to identify the specific contributions each structure in the medial temporal lobe makes towards the formation and storage of long-term declarative memory. The historical background of this work is described including what insights the study of noted neurologic patients H.M. and E.P. provided for understanding the function of the medial temporal lobe. The development of an animal model of medial temporal lobe function is described. Additionally, the insights that lead to the understanding that the brain contains multiple, anatomically discrete, memory systems are described. Finally, three current topics of debate are addressed: First, does the perirhinal cortex exclusively support memory, or does it support both memory and higher order visual perception? Second, is there an anatomical separation between recollection and familiarity? Third, is the organization of spatial memory different between humans and rats, or perhaps the difference is between the working memory capacities of the two species?