Impact of the experimental removal of lizards on Lyme disease risk

The distribution of vector meals in the host community is an important element of understanding and predicting vector-borne disease risk. Lizards (such as the western fence lizard; Sceloporus occidentalis) play a unique role in Lyme disease ecology in the far-western United States. Lizards rather than mammals serve as the blood meal hosts for a large fraction of larval and nymphal western black-legged ticks (Ixodes pacificus--the vector for Lyme disease in that region) but are not competent reservoirs for the pathogen, Borrelia burgdorferi. Prior studies have suggested that the net effect of lizards is to reduce risk of human exposure to Lyme disease, a hypothesis that we tested experimentally. Following experimental removal of lizards, we documented incomplete host switching by larval ticks (5.19%) from lizards to other hosts. Larval tick burdens increased on woodrats, a competent reservoir, but not on deer mice, a less competent pathogen reservoir. However, most larvae failed to find an alternate host. This resulted in significantly lower densities of nymphal ticks the following year. Unexpectedly, the removal of reservoir-incompetent lizards did not cause an increase in nymphal tick infection prevalence. The net result of lizard removal was a decrease in the density of infected nymphal ticks, and therefore a decreased risk to humans of Lyme disease. Our results indicate that an incompetent reservoir for a pathogen may, in fact, increase disease risk through the maintenance of higher vector density and therefore, higher density of infected vectors.     

Climate, deer, rodents, and acorns as determinants of variation in lyme-disease risk

Risk of human exposure to vector-borne zoonotic pathogens is a function of the abundance and infection prevalence of vectors. We assessed the determinants of Lyme-disease risk (density and Borrelia burgdorferi-infection prevalence of nymphal Ixodes scapularis ticks) over 13 y on several field plots within eastern deciduous forests in the epicenter of US Lyme disease (Dutchess County, New York). We used a model comparison approach to simultaneously test the importance of ambient growing-season temperature, precipitation, two indices of deer (Odocoileus virginianus) abundance, and densities of white-footed mice (Peromyscus leucopus), eastern chipmunks (Tamias striatus), and acorns ( Quercus spp.), in both simple and multiple regression models, in predicting entomological risk. Indices of deer abundance had no predictive power, and precipitation in the current year and temperature in the prior year had only weak effects on entomological risk. The strongest predictors of a current year's risk were the prior year's abundance of mice and chipmunks and abundance of acorns 2 y previously. In no case did inclusion of deer or climate variables improve the predictive power of models based on rodents, acorns, or both. We conclude that interannual variation in entomological risk of exposure to Lyme disease is correlated positively with prior abundance of key hosts for the immature stages of the tick vector and with critical food resources for those hosts.     

Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases?

The impact of climate change on vector-borne infectious diseases is currently controversial. In Europe the primary arthropod vectors of zoonotic diseases are ticks, which transmit Borrelia burgdorferi sensu lato (the agent of Lyme disease), tick-borne encephalitis virus and louping ill virus between humans, livestock and wildlife. Ixodes ricinus ticks and reported tick-borne disease cases are currently increasing in the UK. Theories for this include climate change and increasing host abundance. This study aimed to test how I. ricinus tick abundance might be influenced by climate change in Scotland by using altitudinal gradients as a proxy, while also taking into account the effects of hosts, vegetation and weather effects. It was predicted that tick abundance would be higher at lower altitudes (i.e. warmer climates) and increase with host abundance. Surveys were conducted on nine hills in Scotland, all of open moorland habitat. Tick abundance was positively associated with deer abundance, but even after taking this into account, there was a strong negative association of ticks with altitude. This was probably a real climate effect, with temperature (and humidity, i.e. saturation deficit) most likely playing an important role. It could be inferred that ticks may become more abundant at higher altitudes in response to climate warming. This has potential implications for pathogen prevalence such as louping ill virus if tick numbers increase at elevations where competent transmission hosts (red grouse Lagopus lagopus scoticus and mountain hares Lepus timidus) occur in higher numbers.     

No Observed Effect of Landscape Fragmentation on Pathogen Infection Prevalence in Blacklegged Ticks (Ixodes scapularis) in the Northeastern United States

Pathogen prevalence within blacklegged ticks (Ixodes scapularis Say, 1821) tends to vary across sites and geographic regions, but the underlying causes of this variation are not well understood. Efforts to understand the ecology of Lyme disease have led to the proposition that sites with higher host diversity will result in lower disease risk due to an increase in the abundance of inefficient reservoir species relative to the abundance of species that are highly competent reservoirs. Although the Lyme disease transmission cycle is often cited as a model for this “dilution effect hypothesis”, little empirical evidence exists to support that claim. Here we tested the dilution effect hypothesis for two pathogens transmitted by the blacklegged tick along an urban-to-rural gradient in the northeastern United States using landscape fragmentation as a proxy for host biodiversity. Percent impervious surface and habitat fragment size around each site were determined to assess the effect of landscape fragmentation on nymphal blacklegged tick infection with Borrelia burgdorferi and Anaplasma phagocytophilum. Our results do not support the dilution effect hypothesis for either pathogen and are in agreement with the few studies to date that have tested this idea using either a landscape proxy or direct measures of host biodiversity.     

Geographic Risk for Lyme Disease and Human Granulocytic Ehrlichiosis in Southern New York State

Ixodes scapularis, the tick vector of Lyme disease and human granulocytic ehrlichiosis (HGE), is prevalent in much of southern New York state. The distribution of this species has increased, as have reported cases of both Lyme disease and HGE. The unreliability of case reports, however, demonstrates the need for tick and pathogen surveillance in order to accurately define areas of high risk. In this study, a total of 89,550 m² at 34 study sites was drag sampled in 1995 and a total of 51,540 m² at 40 sites was sampled in 1996 to determine tick and pathogen distribution in southern New York state. I. scapularis was collected from 90% of the sites sampled, and regionally, a 2.5-fold increase in nymphal abundance occurred from 1995 to 1996. I. scapularis individuals from all sites were infected with Borrelia burgdorferi in 1995, while an examination of ticks for both B. burgdorferi and the agent of HGE in 1996 confirmed that these organisms were present in all counties; the average coinfection rate was 1.9%. No correlation was found between estimated risk and reported cases of Lyme disease. The geographic disparity of risk observed among sites in this study underscores the need for vector and pathogen surveillance on a regional level. An entomologic risk index can help identify sites for targeted tick control efforts.     

Temporal Distribution of the Annual Nymphal Stock of Ixodes Ricinus Ticks

The human risk of contracting Lyme disease or other tick borne diseases transmitted by the tick species Ixodes ricinus is broadly linked to the tick nymph density. The study was performed in Rambouillet forest (Yvelines, France), a known focus of Lyme borreliosis, from January 1997 to December 1999. We used a nymph sampling methodology which permitted us to obtain a monthly nymph density index (from 0 to 5). Studying the seasonal nymph and larval activity patterns and estimating the larval developmental duration, we demonstrate the existence of an annual nymphal stock. Secondly, we elucidate how this stock is distributed throughout the year, month by month. Its distribution is principally dependent on two factors: the monthly mean ambient temperature and the proportion of active nymphs which find a host each month. Expected monthly nymph densities derived from a theoretical model describing the temperature-dependent stock distribution gave a good fit to the observed densities, accounting for between 76–86% of the monthly variation in observed nymph densities. Predicting the temporal distribution of nymph activity within a stable Lyme borreliosis focus enables more precise identification of risk periods.     

Feeding of Ticks on Animals for Transmission and Xenodiagnosis in Lyme Disease Research

Transmission of the etiologic agent of Lyme disease, Borrelia burgdorferi, occurs by the attachment and blood feeding of Ixodes species ticks on mammalian hosts. In nature, this zoonotic bacterial pathogen may use a variety of reservoir hosts, but the white-footed mouse (Peromyscus leucopus) is the primary reservoir for larval and nymphal ticks in North America. Humans are incidental hosts most frequently infected with B. burgdorferi by the bite of ticks in the nymphal stage. B. burgdorferi adapts to its hosts throughout the enzootic cycle, so the ability to explore the functions of these spirochetes and their effects on mammalian hosts requires the use of tick feeding. In addition, the technique of xenodiagnosis (using the natural vector for detection and recovery of an infectious agent) has been useful in studies of cryptic infection. In order to obtain nymphal ticks that harbor B. burgdorferi, ticks are fed live spirochetes in culture through capillary tubes. Two animal models, mice and nonhuman primates, are most commonly used for Lyme disease studies involving tick feeding. We demonstrate the methods by which these ticks can be fed upon, and recovered from animals for either infection or xenodiagnosis.     

The Lyme Disease Pathogen Has No Effect on the Survival of Its Rodent Reservoir Host

Zoonotic pathogens that cause devastating morbidity and mortality in humans may be relatively harmless in their natural reservoir hosts. The tick-borne bacterium Borrelia burgdorferi causes Lyme disease in humans but few studies have investigated whether this pathogen reduces the fitness of its reservoir hosts under natural conditions. We analyzed four years of capture-mark-recapture (CMR) data on a population of white-footed mice, Peromyscus leucopus, to test whether B. burgdorferi and its tick vector affect the survival of this important reservoir host. We used a multi-state CMR approach to model mouse survival and mouse infection rates as a function of a variety of ecologically relevant explanatory factors. We found no effect of B. burgdorferi infection or tick burden on the survival of P. leucopus. Our estimates of the probability of infection varied by an order of magnitude (0.051 to 0.535) and were consistent with our understanding of Lyme disease in the Northeastern United States. B. burgdorferi establishes a chronic avirulent infection in their rodent reservoir hosts because this pathogen depends on rodent mobility to achieve transmission to its sedentary tick vector. The estimates of B. burgdorferi infection risk will facilitate future theoretical studies on the epidemiology of Lyme disease.     

Geography,Deer, and Host Biodiversity Shape the Pattern of Lyme Disease Emergence in the Thousand Islands Archipelago of Ontario,Canada

In the Thousand Islands region of eastern Ontario, Canada, Lyme disease is emerging as a serious health risk. The factors that influence Lyme disease risk, as measured by the number of blacklegged tick (Ixodes scapularis) vectors infected with Borrelia burgdorferi, are complex and vary across eastern North America. Despite study sites in the Thousand Islands being in close geographic proximity, host communities differed and both the abundance of ticks and the prevalence of B. burgdorferi infection in them varied among sites. Using this archipelago in a natural experiment, we examined the relative importance of various biotic and abiotic factors, including air temperature, vegetation, and host communities on Lyme disease risk in this zone of recent invasion. Deer abundance and temperature at ground level were positively associated with tick abundance, whereas the number of ticks in the environment, the prevalence of B. burgdorferi infection, and the number of infected nymphs all decreased with increasing distance from the United States, the presumed source of this new endemic population of ticks. Higher species richness was associated with a lower number of infected nymphs. However, the relative abundance of Peromyscus leucopus was an important factor in modulating the effects of species richness such that high biodiversity did not always reduce the number of nymphs or the prevalence of B. burgdorferi infection. Our study is one of the first to consider the interaction between the relative abundance of small mammal hosts and species richness in the analysis of the effects of biodiversity on disease risk, providing validation for theoretical models showing both dilution and amplification effects. Insights into the B. burgdorferi transmission cycle in this zone of recent invasion will also help in devising management strategies as this important vector-borne disease expands its range in North America.     

Impact of white‐tailed deer on the spread of Borrelia burgdorferi

There is a public perception that the white‐tailed deer Odocoileus virginianus (Artiodactyla: Cervidae) is the main reservoir supporting the maintenance and spread of the causative agent of Lyme disease, Borrelia burgdorferi. This study examines the pathogen prevalence rate of Borrelia in adult Ixodes scapularis (Ixodida: Ixodidae), the black‐legged tick, collected from white‐tailed deer and compares it with pathogen prevalence rates in adult ticks gathered by dragging vegetation in two contiguous counties west of the Hudson Valley in upstate New York. In both Broome and Chenango Counties, attached and unattached ticks harvested from white‐tailed deer had significantly lower prevalences of B. burgdorferi than those collected from vegetation. No attached ticks on deer (n = 148) in either county, and only 2.4 and 7.3% of unattached ticks (n = 389) in Broome and Chenango Counties, respectively, were harbouring the pathogen. This contrasts with the finding that 40.8% of ticks in Broome County and 46.8% of ticks in Chenango County collected from vegetation harboured the pathogen. These data suggest that a mechanism in white‐tailed deer may aid in clearing the pathogen from attached deer ticks, although white‐tailed deer do contribute to the spatial distribution of deer tick populations and also serve as deadend host breeding sites for ticks.     

Forest fragmentation predicts local scale heterogeneity of Lyme disease risk

Fragmentation of the landscape has been proposed to play an important role in defining local scale heterogeneity in Lyme disease risk through influence on mammalian host density and species composition. We tested this observed relationship in a suburban region around Lyme, Connecticut, where we collected data on the density of the tick vector, Ixodes scapularis and prevalence of the Lyme bacterium, Borrelia burgdorferi at 30 sites. Analysis of the landscape pattern of forest patches was performed using satellite imagery. The calculated landscape indices, which included patch size and isolation, revealed a positive link between fragmentation and both tick density and infection prevalence in ticks. In spite of higher entomologic risk, human incidence of Lyme disease is lower in fragmented contexts suggesting that entomologic risk is not the critical driver of human infections. These results represent a departure from the prior claims that fragmentation and human Lyme disease risk are positively linked. A complete understanding of the influence of landscape fragmentation will allow for improved risk mapping and potential environmental management of Lyme disease.     

Evaluation of the Importance of VlsE Antigenic Variation for the Enzootic Cycle of Borrelia burgdorferi

Efficient acquisition and transmission of Borrelia burgdorferi by the tick vector, and the ability to persistently infect both vector and host, are important elements for the life cycle of the Lyme disease pathogen. Previous work has provided strong evidence implicating the significance of the vls locus for B. burgdorferi persistence. However, studies involving vls mutant clones have thus far only utilized in vitro-grown or host-adapted spirochetes and laboratory strains of mice. Additionally, the effects of vls mutation on tick acquisition and transmission has not yet been tested. Thus, the importance of VlsE antigenic variation for persistent infection of the natural reservoir host, and for the B. burgdorferi enzootic life cycle in general, has not been examined to date. In the current work, Ixodes scapularis and Peromyscus maniculatus were infected with different vls mutant clones to study the importance of the vls locus for the enzootic cycle of the Lyme disease pathogen. The findings highlight the significance of the vls system for long-term infection of the natural reservoir host, and show that VlsE antigenic variability is advantageous for efficient tick acquisition of B. burgdorferi from the mammalian reservoir. The data also indicate that the adaptation state of infecting spirochetes influences B. burgdorferi avoidance from host antibodies, which may be in part due to its respective VlsE expression levels. Overall, the current findings provide the most direct evidence on the importance of VlsE for the enzootic cycle of Lyme disease spirochetes, and underscore the significance of VlsE antigenic variation for maintaining B. burgdorferi in nature.     

Climate impacts on blacklegged tick host-seeking behavior

The nymph of the blacklegged tick (Ixodes scapularis), the primary North American vector of the causative agent of Lyme disease, must attach to a host by the end of its questing season in order to feed and subsequently molt into an adult. The proper timing of this behavior is critical both for the tick’s survival and for perpetuating the transmission of tick-borne pathogens. Questing also depletes limited nymphal lipid reserves and increases desiccation risk. Given this tradeoff, questing behavior and its environmental influences can be expressed in a dynamic state variable model. We develop what we believe to be the first such model for a tick, and investigate the influence of climate on nymph fitness predictions. We apply these results to the hypothesized inland migration of I. scapularis from island refugia, evaluating fitness under suboptimal questing strategies and uncertain environmental conditions.     

Real-Time PCR for Simultaneous Detection and Quantification of Borrelia burgdorferi in Field-Collected Ixodes scapularis Ticks from the Northeastern United States

The density of spirochetes in field-collected or experimentally infected ticks is estimated mainly by assays based on microscopy. In this study, a real-time quantitative PCR (qPCR) protocol targeting the Borrelia burgdorferi-specific recA gene was adapted for use with a Lightcycler for rapid detection and quantification of the Lyme disease spirochete, B. burgdorferi, in field-collected Ixodes scapularis ticks. The sensitivity of qPCR for detection of B. burgdorferi DNA in infected ticks was comparable to that of a well-established nested PCR targeting the 16S-23S rRNA spacer. Of the 498 I. scapularis ticks collected from four northeastern states (Rhode Island, Connecticut, New York, and New Jersey), 91 of 438 (20.7%) nymphal ticks and 15 of 60 (25.0%) adult ticks were positive by qPCR assay. The number of spirochetes in individual ticks varied from 25 to 197,200 with a mean of 1,964 spirochetes per nymphal tick and a mean of 5,351 spirochetes per adult tick. No significant differences were found in the mean numbers of spirochetes counted either in nymphal ticks collected at different locations in these four states (P = 0.23 by one-way analysis of variance test) or in ticks infected with the three distinct ribosomal spacer restriction fragment length polymorphism types of B. burgdorferi (P = 0.39). A high degree of spirochete aggregation among infected ticks (variance-to-mean ratio of 24,877; moment estimate of k = 0.279) was observed. From the frequency distribution data and previously published transmission studies, we estimated that a minimum of 300 organisms may be required in a host-seeking nymphal tick to be able to transmit infection to mice while feeding on mice. These data indicate that real-time qPCR is a reliable approach for simultaneous detection and quantification of B. burgdorferi infection in field-collected ticks and can be used for ecological and epidemiological surveillance of Lyme disease spirochetes.     

Disease Risk & Landscape Attributes of Tick-Borne Borrelia Pathogens in the San Francisco Bay Area,California

Habitat heterogeneity influences pathogen ecology by affecting vector abundance and the reservoir host communities. We investigated spatial patterns of disease risk for two human pathogens in the Borrelia genus–B. burgdorferi and B. miyamotoi–that are transmitted by the western black-legged tick, Ixodes pacificus. We collected ticks (349 nymphs, 273 adults) at 20 sites in the San Francisco Bay Area, California, USA. Tick abundance, pathogen prevalence and density of infected nymphs varied widely across sites and habitat type, though nymphal western black-legged ticks were more frequently found, and were more abundant in coast live oak forest and desert/semi-desert scrub (dominated by California sagebrush) habitats. We observed Borrelia infections in ticks at all sites where we able to collect >10 ticks. The recently recognized human pathogen, B. miyamotoi, was observed at a higher prevalence (13/349 nymphs = 3.7%, 95% CI = 2.0–6.3; 5/273 adults = 1.8%, 95% CI = 0.6–4.2) than recent studies from nearby locations (Alameda County, east of the San Francisco Bay), demonstrating that tick-borne disease risk and ecology can vary substantially at small geographic scales, with consequences for public health and disease diagnosis.     

Vectorial capacity of North American Ixodes ticks.

Ixodes dammini, the vector of Lyme disease and babesiosis, is distributed in various locations in the northeastern quadrant of the United States and nearby Canada. The life cycle of this tick, which includes larval, nymphal, and adult stages, spans at least two years. The tick over-winters between larval and nymphal feeding. Horizontal transmission of pathogens is facilitated by a feeding pattern in which both the larval and nymphal stages feed on the white-footed mouse, Peromyscus leucopus, and by a seasonal pattern of activity in which nymphs precede larvae. The species range appears to have expanded from a single island location, and has invaded new sites since the 1940s, some as recently as 1980. This increased abundance appears to be related to the increased abundance of deer, the preferred host of the adult stage. I. muris predominated in coastal Massachusetts before I. dammini became abundant, but is probably now extinct. I. scapularis, which is present in the southern U.S., is a poor vector of mouse parasites because about 90 percent of these immature ticks feed on lizards. To the extent that horizontal transmission occurs, we suggest that mice serve as the principal reservoir for the Lyme spirochete as well as Babesia microti.     

Density of deer in relation to the prevalence of Borrelia burgdorferi s.1. in Ixodes ricinus nymphs in Rambouillet forest, France

The Rambouillet Forest, a Lyme disease-endemic area near Paris, France, was surveyed from September 1994 to October 1995 to determine the risk periods and zones for humans. Firstly, during the period of Ixodes ricinus activity, abundance of nymphs is greater in spring than in autumn. Secondly, we observed significant variation in nymphal abundance between zones according to the density of cervids. The polymerase chain reaction (PCR) was used to detect DNA of Borrelia burgdorferi sensu lato in 461 unfed nymphs. DNA was detected in 38 nymphs (8.2%). By genospecific PCR based on the OspA gene, we detected the three pathogenic spirochetes with occurrences of 10.3, 31.1 and 58.6 for B. burgdorferi s.s., Borrelia garinii and Borrelia afzelii, respectively, indicating that B. afzelii is probably the main Borrelia species in the Rambouillet Forest. Finally, 11.5% of positive nymphs exhibited a double infection. Infection rates of I. ricinus nymphs by B. burgdorferi s.l. were not significantly different throughout the year for a given area, indicating that the risk periods of acquiring Lyme disease are mainly linked to nymph activity and correspond to spring and autumn. Likewise infection rates of nymphs were not significantly different between zones with a high density of deer (more than 100 animals per 100 ha) and zones with lower deer density (less than 20 animals per 100 ha). In addition to the role of deer as an amplifier of tick populations, these data indicate that zones with a high density of cervids should be considered as higher risk areas. © Rapid Science Ltd. 1998     

The spatial distribution of Borrelia burgdorferi-infected Ixodes ricinus in the Connemara region of County Galway,Ireland

Studies were carried out in the Connemara area of County Galway in the west of Ireland in order to determine the abundance and distribution of the tick, Ixodes ricinus and the prevalence of its infection with Borrelia burgdorferi. The tick was very abundant locally, in particular when associated with cattle, sheep and enclosed red deer. Large numbers of ticks not only occurred on the pastures, but also on adjacent roadside verges. No infections with B. burgdorferi could be demonstrated when nymphal ticks were sampled from central areas of the pastures, suggesting that livestock and red deer are probably not significant reservoirs of the spirochaete. Small numbers of infected nymphal and adult ticks were associated with hedges, dry stone walls, the margins of woodland adjoining infested pastures and in woodland from which livestock were excluded. Woodmice (Apodemus sylvaticus) were most numerous in such habitats and the majority were infected with B. burgdorferi.     

Large Scale Spatial Risk and Comparative Prevalence of Borrelia miyamotoi and Borrelia burgdorferi Sensu Lato in Ixodes pacificus

Borrelia miyamotoi is a newly described emerging pathogen transmitted to people by Ixodes species ticks and found in temperate regions of North America, Europe, and Asia. There is limited understanding of large scale entomological risk patterns of B. miyamotoi and of Borreila burgdorferi sensu stricto (ss), the agent of Lyme disease, in western North America. In this study, B. miyamotoi, a relapsing fever spirochete, was detected in adult (n = 70) and nymphal (n = 36) Ixodes pacificus ticks collected from 24 of 48 California counties that were surveyed over a 13 year period. Statewide prevalence of B. burgdorferi sensu lato (sl), which includes B. burgdorferi ss, and B. miyamotoi were similar in adult I. pacificus (0.6% and 0.8%, respectively). In contrast, the prevalence of B. burgdorferi sl was almost 2.5 times higher than B. miyamotoi in nymphal I. pacificus (3.2% versus 1.4%). These results suggest similar risk of exposure to B. burgdorferi sl and B. miyamotoi from adult I. pacificus tick bites in California, but a higher risk of contracting B. burgdorferi sl than B. miyamotoi from nymphal tick bites. While regional risk of exposure to these two spirochetes varies, the highest risk for both species is found in north and central coastal California and the Sierra Nevada foothill region, and the lowest risk is in southern California; nevertheless, tick-bite avoidance measures should be implemented in all regions of California. This is the first study to comprehensively evaluate entomologic risk for B. miyamotoi and B. burgdorferi for both adult and nymphal I. pacificus, an important human biting tick in western North America.     

Controlling tick-borne diseases through domestic animal management: a theoretical approach

Vector-borne diseases are of global importance to human and animal health. Empirical trials of effective methods to control vectors and their pathogens can be difficult for practical, financial and ethical reasons. Here, therefore, we use a mathematical model to predict the effectiveness of a vector-borne disease control method. As a case study, we use the tick-louping ill virus system, where sheep are treated with acaricide in an attempt to control ticks and disease in red grouse , an economically important game bird. We ran the model under different scenarios of sheep flock sizes, alternative host (deer) densities, acaricide efficacies and tick burdens. The model predicted that, with very low deer densities, using sheep as tick mops can reduce the tick population and virus prevalence. However, treatment is ineffective above a certain threshold deer density, dependent on the comparative tick burden on sheep and deer. The model also predicted that high efficacy levels of acaricide must be maintained for effective tick control. This study suggests that benignly managing one host species to protect another host species from a vector and pathogen can be effective under certain conditions. It also highlights the importance of understanding the ecological complexity of a system, in order to target control methods only under certain circumstances for maximum effectiveness.