Leveraging satellite observations to reveal ecological drivers of pest densities across landscapes.

Landscape ecologists have long suggested that pest abundances increase in simplified, monoculture landscapes. However, tests of this theory often fail to predict pest population sizes in real-world agricultural fields. These failures may arise not only from variation in pest ecology, but also from the widespread use of categorical land-use maps that do not adequately characterize habitat-availability for pests. We used 1163 field-year observations of Lygus hesperus (Western Tarnished Plant Bug) densities in California cotton fields to determine whether integrating remotely-sensed metrics of vegetation productivity and phenology into pest models could improve pest abundance analysis and prediction. Because L. hesperus often overwinters in non-crop vegetation, we predicted that pest abundances would peak on farms surrounded by more non-crop vegetation, especially when the non-crop vegetation is initially productive but then dries down early in the year, causing the pest to disperse into cotton fields. We found that the effect of non-crop habitat on pest densities varied across latitudes, with a positive relationship in the north and a negative one in the south. Aligning with our hypotheses, models predicted that L. hesperus densities were 35 times higher on farms surrounded by high versus low productivity non-crop vegetation (EVI area 350 vs. 50) and 2.8 times higher when dormancy occurred earlier versus later in the year (May 15 vs. June 30). Despite these strong and significant effects, we found that integrating these remote-sensing variables into land-use models only marginally improved pest density predictions in cotton compared to models with categorical land cover metrics alone. Together, our work suggests that the remote sensing variables analyzed here can advance our understanding of pest ecology, but not yet substantively increase the accuracy of pest abundance predictions.

A test of balanced fitness limitations theory: Pollen limitation in plants.

When reproductive success is determined by the relative availabilities of a series of essential, non-substitutable resources, the theory of balanced fitness limitations predicts that the cost of harvesting a particular resource shapes the likelihood that a shortfall of that resource will constrain realized fitness. Plant reproduction through female function offers a special opportunity to test this theory; essential resources in this context include, first, the pollen received from pollinators or abiotic vectors that is used to fertilize ovules, and, second, the resources needed to provision the developing seeds and fruit. For many plants realized reproductive success through female function can be readily quantified in the field, and one key potential constraint on fitness, pollen limitation, can be assessed experimentally by manually supplementing pollen receipt. We assembled a comparative dataset of pollen limitation using only studies that supplement pollen to all flowers produced over the plant's reproductive lifespan. Pre- and post-pollination costs were estimated using the weight of flowers and fruits and estimates of fruit set. Consistent with expectations, we find self-incompatible plants make greater pre-pollination investments and experience greater pollen limitation. However, contrary to theoretical expectations, when variation due to self-compatibility is accounted for by including self-compatibility in the statistical model as a covariate, we find no support for the prediction that plants that invest more heavily in pre-pollination costs are subject to greater pollen limitation. Strong within-species, between-population variation in the expression of pollen limitation makes the quantification of mean pollen limitation difficult. We urge plant ecologists to conduct more studies of pollen limitation using whole-plant pollen supplementation to produce a richer comparative dataset that would support a more robust test of the balanced limitations hypothesis.

Increasing crop field size does not consistently exacerbate insect pest problems.

Increasing diversity on farms can enhance many key ecosystem services to and from agriculture, and natural control of arthropod pests is often presumed to be among them. The expectation that increasing the size of monocultural crop plantings exacerbates the impact of pests is common throughout the agroecological literature. However, the theoretical basis for this expectation is uncertain; mechanistic mathematical models suggest instead that increasing field size can have positive, negative, neutral, or even nonlinear effects on arthropod pest densities. Here, we report a broad survey of crop field-size effects: across 14 pest species, 5 crops, and 20,000 field years of observations, we quantify the impact of field size on pest densities, pesticide applications, and crop yield. We find no evidence that larger fields cause consistently worse pest impacts. The most common outcome (9 of 14 species) was for pest severity to be independent of field size; larger fields resulted in less severe pest problems for four species, and only one species exhibited the expected trend of larger fields worsening pest severity. Importantly, pest responses to field size strongly correlated with their responses to the fraction of the surrounding landscape planted to the focal crop, suggesting that shared ecological processes produce parallel responses to crop simplification across spatial scales. We conclude that the idea that larger field sizes consistently disrupt natural pest control services is without foundation in either the theoretical or empirical record.

Pathways to the density-dependent expression of cannibalism, and consequences for regulated population dynamics.

Cannibalism, once viewed as a rare or aberrant behavior, is now recognized to be widespread and to contribute broadly to the self-regulation of many populations. Cannibalism can produce endogenous negative feedback on population growth because it is expressed as a conditional behavior, responding to the deteriorating ecological conditions that flow, directly or indirectly, from increasing densities of conspecifics. Thus, cannibalism emerges as a strongly density-dependent source of mortality. In this synthesis, we review recent research that has revealed a rich diversity of pathways through which rising density elicits increased cannibalism, including both factors that (a) elevate the rate of dangerous encounters between conspecifics and (b) enhance the likelihood that such encounters will lead to successful cannibalistic attacks. These pathways include both features of the autecology of cannibal populations and features of interactions with other species, including food resources and pathogens. Using mathematical models, we explore the consequences of including density-dependent cannibal attack rates on population dynamics. The conditional expression of cannibalism generally enhances stability and population regulation in single-species models but also may increase opportunities for alternative states and prey population escape from control by cannibalistic predators.

A double-edged sword: parental care increases risk of offspring infection by a maternally vectored parasite.

Parental care can protect offspring from predators but can also create opportunities for parents to vector parasites to their offspring. We hypothesized that the risk of infection by maternally vectored parasites would increase with the frequency of mother-offspring contact. Ammophila spp. wasps (Hymenoptera: Sphecidae) build nests in which they rear a single offspring. Ammophila species exhibit varied offspring provisioning behaviours: some species enter the nest once to provision a single, large caterpillar, whereas others enter the nest repeatedly to provision with many smaller caterpillars. We hypothesized that each nest visit increases the risk of offspring parasitism by Paraxenos lugubris (Strepsiptera: Xenidae), whose infectious stages ride on the mother wasp (phoresy) to reach the vulnerable Ammophila offspring. We quantified parasitism risk by external examination of museum-curated Ammophila specimens-the anterior portion of P. lugubris protrudes between the adult host's abdominal sclerites and reflects infection during the larval stage. As predicted, Ammophila species that receive larger numbers of provisions incur greater risks of parasitism, with nest provisioning behaviour explaining ca 90% of the interspecific variation in mean parasitism. These findings demonstrate that parental care can augment, rather than reduce, the risk of parasite transmission to offspring.

Herbivory by European Earwigs (Forficula auricularia; Dermaptera: Forficulidae) on Citrus Species Commonly Cultivated in California.

Agricultural plant species differ in susceptibility to herbivores; therefore, identifying natural resistances or tolerances to pests can be leveraged to develop preventative, integrated pest management approaches. While many Citrus species are grown in California, most pest management guidelines are based upon research conducted on navel oranges [Citrus sinensis (L.) Osbeck; Sapindales: Rutaceae]. A recent study has established European earwigs (Forficula auricularia L.; Dermaptera: Forficulidae) as herbivores of young navel orange fruit, causing damage ranging from small bite marks to large chewed holes. It is unknown whether earwigs damage fruit of other citrus species. We conducted field experiments in which we caged earwigs to branch terminals bearing young fruit to explore potential differences in susceptibility of Citrus species to European earwigs. Specifically, we tested whether three species, navel oranges, clementines (C. clementina hort. ex Tanaka), and true mandarins (C. reticulata Blanco) exhibit differences in: 1) feeding deterrence to earwigs; 2) suitability as food for earwigs; 3) preferential abscission of damaged fruit; and 4) healing of damaged fruit. Earwigs caused heavy damage on navel orange and clementine fruit, whereas heavy damage was rare on true mandarin fruit. There was little evidence of preferential abscission of damaged fruit or healing of seriously damaged fruit. Consequently, several heavily damaged navel orange and one clementine fruit were retained to harvest and developed large scars. Overall, we found that Citrus fruit vary in their susceptibility to earwigs, and pest management strategies for earwigs should be refined to consider their varying effects on different Citrus species.

The causes and consequences of pest population variability in agricultural landscapes.

Variability in population densities is key to the ecology of natural systems but also has great implications for agriculture. Farmers' decisions are heavily influenced by their risk aversion to pest outbreaks that result in major yield losses. However, the need for long-term pest population data across many farms has prevented researchers from exploring the drivers and implications of pest population variability (PV). Here, we demonstrate the critical importance of PV for sustainable farming by analyzing 13 years of pest densities across >1300 Spanish olive groves and vineyards. Variable populations were more likely to cause major yield losses, but also occasionally created temporal windows when densities fell below insecticide spray thresholds. Importantly, environmental factors regulating pest variability were very distinct from factors regulating mean density, suggesting variability needs to be uniquely managed. Finally, we found diversifying landscapes may be a win-win situation for conservation and farmers, as diversified landscapes promote less abundant and less variable pest populations. Therefore, we encourage agricultural stakeholders to increase the complexity of the landscapes surrounding their farms through conserving/restoring natural habitat and/or diversifying crops.

Characterizing Herbivory by European Earwigs (Dermaptera: Forficulidae) on Navel Orange Fruit with Comparison to Forktailed Bush Katydid (Orthoptera: Tettigoniidae) Herbivory.

In establishing Integrated Pest Management (IPM) plans for understudied pests, it is crucial to understand the nature of their herbivory and resulting damage. European earwig (Forficula auricularia L.; Dermaptera: Forficulidae) densities are increasing in citrus orchards in Central California. Field observations suggest that earwigs feed on young, developing citrus fruit, but this hypothesis had not been examined with formal experimentation. Forktailed bush katydid nymphs (Scudderia furcata Brunner von Wattenwyl; Orthoptera: Tettigoniidae) are well-known citrus herbivores that feed on young citrus fruit, and it is possible that earwig damage may be misdiagnosed as katydid damage. Here we report findings from two field experiments in navel oranges (Citrus sinensis (L.) Osbeck; Sapindales: Rutaceae) that together tested: (1) whether earwigs damage young citrus fruit; (2) whether the amount of damage earwigs generate differs across developmental stage or sex of adult earwigs; (3) the window of time during which fruit are most sensitive to earwig damage; (4) whether damaged fruit are retained to harvest; and (5) the resulting damage morphology caused by earwigs relative to katydids. Earwigs, particularly nymphs, chewed deep holes in young citrus fruit from 0 to 3 wk after petal fall. Fruit damaged by earwigs were retained and exhibited scars at harvest. The morphology and distribution of scars on mature fruit only subtly differed between earwigs and katydids. This study establishes that earwigs can be direct pests in mature navel orange trees by generating scars on fruit and likely contribute to fruit quality downgrades.

Evaluating the Quality of Ecoinformatics Data Derived From Commercial Agriculture: A Repeatability Analysis of Pest Density Estimates.

Each year, consultants and field scouts working in commercial agriculture undertake a massive, decentralized data collection effort as they monitor insect populations to make real-time pest management decisions. These data, if integrated into a database, offer rich opportunities for applying big data or ecoinformatics methods in agricultural entomology research. However, questions have been raised about whether or not the underlying quality of these data is sufficiently high to be a foundation for robust research. Here I suggest that repeatability analysis can be used to quantify the quality of data collected from commercial field scouting, without requiring any additional data gathering by researchers. In this context, repeatability quantifies the proportion of total variance across all insect density estimates that is explained by differences across populations and is thus a measure of the underlying reliability of observations. Repeatability was moderately high for cotton fields scouted commercially for total Lygus hesperus Knight densities (R = 0.631) and further improved by accounting for observer effects (R = 0.697). Repeatabilities appeared to be somewhat lower than those computed for a comparable, but much smaller, researcher-generated data set. In general, the much larger sizes of ecoinformatics data sets are likely to more than compensate for modest reductions in measurement precision. Tools for evaluating data quality are important for building confidence in the growing applications of ecoinformatics methods.

Control Failures Following Insecticide Applications in Commercial Agriculture: How Often Do They Occur? A Case Study of Lygus hesperus (Hemiptera: Miridae) Control in Cotton.

Although surveys of pest populations documenting evolved insecticide resistance often suggest abundant potential for insecticide control failures, studies documenting the actual occurrence of such failures in commercial agriculture are rare. If farmers currently practice adaptive management, abandoning the use of insecticides once resistance emerges, actual control failures could be rare. Here I use data gathered by independent pest management consultants to describe a case study of the realized efficacy of commercial field applications of insecticides, examining the control of Lygus hesperus Knight on cotton. On average, insecticides reduced target pest populations to 19% of their preapplication densities. Short-term efficacy of insecticides was variable, but only one severe control failure was observed (1 of 50, 2%). The rarity of severe control failures observed in this study is in agreement with the few other studies conducted in commercial settings, but additional research is needed to assess the generality of this result. Although pesticides can cause longer-term problems, including target pest resurgences and secondary pest outbreaks, risk-averse attitudes among farmers coupled with relatively consistent short-term insecticide efficacy may be potent forces propelling farmers toward the use of insecticides.

Profile of Fork-Tailed Bush Katydid (Orthoptera: Tettigoniidae) Feeding on Fruit of Clementine Mandarins.

Sweet oranges (Citrus sinensis (L.) Osbeck Sapindales: Rutaceae) dominated commercial citrus production in California until recently when there has been a shift to mandarins, mostly Citrus reticulata (Blanco) mandarins and Citrus clementina (hort. ex Tanaka) clementines. Past analyses of commercial field scouting and harvest data indicated that fork-tailed bush katydids (Scudderia furcata Brunner von Wattenwyl), a major pest in oranges, are present in clementine groves, but that fruit scarring attributed to katydids is rare. Conversely, jagged or web-like scarring attributed to caterpillars was more prevalent than expected. We used two field experiments in four representative cultivars of clementines to test four explanatory hypotheses for this observation: 1) katydids do not feed on clementine fruit, 2) damaged clementine fruit recover, 3) damaged clementine fruit preferentially abscise, and 4) katydid scars on clementine fruit have a different, undocumented morphology, not recognized as katydid damage. We find support for the latter two hypotheses. Katydids fed readily on the clementine fruit of all cultivars tested, chewing irregular holes that developed into jagged or web-like scars of a range of shapes and often led to splitting and abscission of maturing fruit. The katydid scars often more closely resembled chewing caterpillar damage than the round katydid scars in oranges, suggesting that katydid damage is being misclassified in clementines. The resistance documented in some other mandarins was not observed. Katydids are clearly a frugivorous pest causing previously unrecognized scarring in clementines.

Landscape simplification increases vineyard pest outbreaks and insecticide use.

Diversifying agricultural landscapes may mitigate biodiversity declines and improve pest management. Yet landscapes are rarely managed to suppress pests, in part because researchers seldom measure key variables related to pest outbreaks and insecticides that drive management decisions. We used a 13-year government database to analyse landscape effects on European grapevine moth (Lobesia botrana) outbreaks and insecticides across c. 400 Spanish vineyards. At harvest, we found pest outbreaks increased four-fold in simplified, vineyard-dominated landscapes compared to complex landscapes in which vineyards are surrounded by semi-natural habitats. Similarly, insecticide applications doubled in vineyard-dominated landscapes but declined in vineyards surrounded by shrubland. Importantly, pest population stochasticity would have masked these large effects if numbers of study sites and years were reduced to typical levels in landscape pest-control studies. Our results suggest increasing landscape complexity may mitigate pest populations and insecticide applications. Habitat conservation represents an economically and environmentally sound approach for achieving sustainable grape production.

Phylogenetic escape from pests reduces pesticides on some crop plants.

Pesticides are a ubiquitous component of conventional crop production but come with considerable economic and ecological costs. We tested the hypothesis that variation in pesticide use among crop species is a function of crop economics and the phylogenetic relationship of a crop to native plants because unrelated crops accrue fewer herbivores and pathogens. Comparative analyses of a dataset of 93 Californian crops showed that more valuable crops and crops with close relatives in the native plant flora received greater pesticide use, explaining roughly half of the variance in pesticide use among crops against pathogens and herbivores. Phylogenetic escape from arthropod and pathogen pests results in lower pesticides, suggesting that the introduced status of some crops can be leveraged to reduce pesticides.

Bugs scaring bugs: enemy-risk effects in biological control systems.

Enemy-risk effects, often referred to as non-consumptive effects (NCEs), are an important feature of predator-prey ecology, but their significance has had little impact on the conceptual underpinning or practice of biological control. We provide an overview of enemy-risk effects in predator-prey interactions, discuss ways in which risk effects may impact biocontrol programs and suggest avenues for further integration of natural enemy ecology and integrated pest management. Enemy-risk effects can have important influences on different stages of biological control programs, including natural enemy selection, efficacy testing and quantification of non-target impacts. Enemy-risk effects can also shape the interactions of biological control with other pest management practices. Biocontrol systems also provide community ecologists with some of the richest examples of behaviourally mediated trophic cascades and demonstrations of how enemy-risk effects play out among species with no shared evolutionary history, important topics for invasion biology and conservation. We conclude that the longstanding use of ecological theory by biocontrol practitioners should be expanded to incorporate enemy-risk effects, and that community ecologists will find many opportunities to study enemy-risk effects in biocontrol settings.

Arthropod Infestation Levels on Mandarins in California.

Integrated pest management (IPM) guidelines for horticulture are typically established from years of experimental research and experience for a crop species. Ecoinformatics methods can help to quickly adapt these guidelines following major changes in growing practices. Citrus production in California is facing several major challenges, one of which is a shift away from sweet oranges [Citrus sinensis (L.) Osbeck Sapindales: Rutaceae] toward mandarins (including mostly cultivars of C. reticulata Blanco and C. clementina hort. ex Tanaka). In the absence of IPM guidelines for mandarins, growers are relying on pest information developed from oranges. We mined a database of management records from commercial growers and consultants to determine densities for four arthropod pests: cottony cushion scale (Icerya purchasi Maskell Hemiptera: Monophlebidae), citricola scale (Coccus pseudomagnoliarum Kuwana Hemiptera: Coccidae), European earwig (Forficula auricularia Linnaeus Dermaptera: Forficulidae), citrus red mite (Panonychus citri McGregor Acari: Tetranychidae), and a natural enemy, predatory mites in the genus Euseius (Congdon Acarina: Phytoseiidae). Densities of cottony cushion scale were approximately 10-40 times higher in the two most commonly grown mandarin species than in sweet oranges, suggesting this pest is reaching outbreak levels more often on mandarins. Densities of the other pests and predatory mites did not differ significantly across citrus species. This is a first step toward establishing IPM guidelines for mandarins for these pests; more research is needed to determine how arthropod densities relate to crop performance in mandarins.

Variation in pesticide use across crops in California agriculture: Economic and ecological drivers.

Pesticide use is a key component of efficient crop production, but is associated with a suite of costs. Understanding the main drivers of pesticide use will help us target research to develop effective alternatives. Although economic models predict, and empirical tests confirm, that the value of the crop being protected is an important determinant of between-crop variation in pesticide use, previous tests of this prediction have examined only modest numbers of crops and have not assessed the relative importance of crop value versus ecological determinants of pesticide use. Here we analyze variation in pesticide use across 93 crops grown in California, USA. We examine the joint roles of crop value and ecological determinants of pesticide use, including (i) the number of pest species associated with each crop; (ii) the distinction between annual vs. perennial crops; and (iii) the distinction between unprocessed vs. processed crops. As predicted, crop value was the dominant driver of the use of pesticides directed at arthropods and at plant pathogens, explaining 52.7% and 54.6% of total deviance, respectively. Ecological determinants of pesticide use were, however, also detected. Pesticide use was greater on crops that hosted a larger number of arthropod pest species (r = 0.32) or plant pathogen species (r = 0.29); for these pest groups, we saw no differences in pesticide use between annual vs. perennial crops, or processed vs. unprocessed crops. Perhaps surprisingly, crop value failed to explain the substantial between-crop variation in use of pesticides targeting weeds (1.7% of deviance explained, n.s.). Instead, an ecological factor, whether the crop was an annual versus a perennial plant, was the most important predictor of pesticide use against weeds, with more frequent applications on perennial crops. We conclude that both economic and ecological drivers influence the magnitude of potential crop losses, thereby shaping farmer pest control practices.

Resistance of Fruits From a Mandarin Cultivar to Feeding by Fork-Tailed Bush Katydids.

Plants use a variety of mechanisms to defend against herbivore damage, each with different consequences for agricultural production. Crops relying on tolerance strategies may need different pest management approaches versus those relying on resistance strategies. Previous work suggested that densities of fork-tailed bush katydids (Scudderia furcata Brunner von Wattenwyl [Orthoptera: Tettigoniidae]) that generated substantial scarring on cultivars of sweet oranges (Citrus sinensis, (L.) Osbeck [Sapindales: Rutaceae]) produced only low levels of scarring on cultivars of Citrus reticulata Blanco mandarins. We used field experiments in representative cultivars of these species to test non-mutually exclusive hypotheses regarding the mechanisms underlying this observation: 1) katydids are averse to feeding on mandarin fruits, 2) damaged mandarin fruits preferentially abscise, 3) damaged mandarin fruit tissue recovers during development, and 4) katydid scars on mandarins have a different morphology that may result in misclassification. We found strong support for the first hypothesis, demonstrating that katydids reject opportunities to feed on C. reticulata fruit. Instead of chewing deep holes in the fruit, as was commonly observed for C. sinensis, the katydids only scratched the surface of the C. reticulata fruits. The hypotheses of preferential abscission of damaged fruits and of recovery of damaged tissue were not supported. The low incidence of damage to the mandarins prevented a comprehensive assessment of the scar morphology; however, at harvest, the superficial cuts in C. reticulata were not easily distinguishable from background damage. This indicates that in contrast to C. sinensis, C. reticulata has substantial natural resistance to fork-tailed bush katydids making them a non-pest in this crop.

Differential Impacts of Citrus Thrips Across Sweet Orange and Mandarin Species.

Several domesticated Citrus species are grown as major commercial crops in California. Despite this, farmers currently use a single set of management practices, originally created for sweet oranges (Citrus sinensis (L.) Osbeck [Sapindales: Rutaceae]), for both sweet oranges and all mandarin species. Mandarins, primarily Citrus reticulata Blanco, Citrus clementina hort. ex Tanaka, and Citrus unshiu Marcovitch, comprise almost 25% of California citrus acreage, and little work has been done to assess host-pest interactions for these species. Citrus thrips (Scirtothripscitri Moulton [Thysanoptera: Thripidae]) are one of the main pests in California citrus and are major targets for early spring, "petal fall" insecticide applications. We used mixed species citrus blocks to test the influence of Citrus species, including C. sinensis, C. reticulata, C. clementina, and C. unshiu, on 1) citrus thrips densities following petal fall; 2) citrus thrips-induced scarring on both the calyx and stylar ends of fruit; and 3) fruit deformation. Citrus sinensis and C. unshiu had relatively high citrus thrips densities and scarring levels, whereas C. reticulata had lower densities of citrus thrips and scarring levels. The age structure of citrus thrips populations also varied across Citrus species. Fruit deformity associated with citrus thrips scarring was found on all Citrus species examined. Scarring on the stylar-end of fruit, a previously largely ignored location of citrus thrips scarring, was found to be common in C. reticulata. It is clear from our work that species-specific management guidelines for citrus thrips are needed in sweet oranges and mandarins.

Disease, contagious cannibalism, and associated population crash in an omnivorous bug, Geocoris pallens.

Disease and cannibalism are two strongly density-dependent processes that can suppress predator populations. Here we show that California populations of the omnivorous predatory bug Geocoris pallens are subject to infection by a pathogen, as yet unidentified, that elicits elevated expression of cannibalism. Laboratory experiments showed that the pathogen is moderately virulent, causing flattened abdomens, elevated nymphal mortality, delayed development, and reduced body size of adult females. Infection furthermore increases the expression of cannibalism. Field populations of Geocoris spp. declined strongly in association with sharp increases in the expression of egg cannibalism by adult G. pallens. Increased cannibalism was accompanied by a strongly bimodal distribution of cannibalism expression, with some females (putatively uninfected) expressing little cannibalism and others (putatively infected) consuming most or all of the eggs present. Highly cannibalistic females did not increase their consumption of Ephestia cautella moth eggs, suggesting that the high cannibalism phenotype reflected a specific loss of restraint against eating conspecifics. Highly cannibalistic females also often exhibited reduced egg laying, consistent with a virulent pathogen; less frequently, more cannibalistic females exhibited elevated egg laying, suggesting that cannibalism might also facilitate recycling of nutrients in eggs. Elevated cannibalism was not correlated with reduced prey availability or elevated field densities of G. pallens. Geocoris pallens population crashes appear to reflect the combined consequences of direct virulence-adverse pathogen effects on the infected host's physiology-and indirect virulence-mortality of both infected and uninfected individuals due to elevated cannibalism expression by infected individuals.