Influence of host migration between woodland and pasture on the population dynamics of the tick Ixodes ricinus: A modelling approach

Ticks act as vectors of pathogens that can be harmful to animals and/or humans. Epidemiological models can be useful tools to investigate the potential effects of control strategies on diseases such as tick-borne diseases. The modelling of tick population dynamics is a prerequisite to simulating tick-borne diseases and the corresponding spread of the pathogen. We have developed a dynamic model to simulate changes in tick density at different stages (egg, larva, nymph and adult) under the influence of temperature. We have focused on the tick Ixodes ricinus, which is widespread in Europe. The main processes governing the biological cycles of ticks were taken into account: egg laying, hatching, development, host (small, mainly rodents, or large, like deer and cattle, mammals) questing, feeding and mortality. This model was first applied to a homogeneous habitat, where simulations showed the ability of the model to reproduce the general patterns of tick population dynamics. We considered thereafter a multi-habitat model, where three different habitats (woodland, ecotone and meadow) were connected through host migration. Based on this second application, it appears that migration from woodland, via the ecotone, is necessary to sustain the presence of ticks in the meadow. Woodland can therefore be considered as a source of ticks for the meadow, which in turn can be regarded as a sink. The influence of woodland on surrounding tick densities increases in line with the area of this habitat before reaching a plateau. A sensitivity analysis to parameter values was carried out and demonstrated that demographic parameters (sex ratio, development, mortality during feeding and questing, host finding) played a crucial role in the determination of questing nymph densities. This type of modelling approach provides insight into the influence of spatial heterogeneity on tick population dynamics.     

Microclimate influence in a physiological model of cattle-fever tick (Boophilus spp.) population dynamics

Since their official eradication from the US in 1943, the cattle-tick species Boophilus microplus and Boophilus annulatus, vectors of bovine babesiosis, frequently have penetrated a quarantine zone established along the Texas–Mexico border designed to exclude them. Inspection and quarantine procedures have eradicated reinfestations successfully within the US, but increasing acaricide resistance in Mexican B. microplus populations poses a threat to future eradication efforts. Better understanding of interrelationships among Boophilus populations, their hosts, and vegetation communities in south Texas could improve prediction of the behavior of reintroduced Boophilus populations and increase management options. To this end, we constructed a simulation model to evaluate how microclimate, habitat (i.e. vegetation) heterogeneity, and within-pasture cattle movement may influence dynamics of Boophilus ticks in south Texas. Unlike previous Boophilus tick models, this model simulates dynamics at an hourly time-step, calculates all off-host dynamics as functions of temperature and relative humidity, and runs with ground-level microclimate data collected bi-hourly in three different habitat types. Sensitivity analysis of the model showed that temperatures and relative humidities created by habitat type, as well as engorged female mass, influenced tick population dynamics most strongly. Host habitat selection, initial number of larvae per cow, and the number of cells into which the simulated pasture was divided also had a strong influence. Population dynamics appeared moderately sensitive to the proportion of Bos indicus in cattle genotypes and the larval attachment rate, while appearing relatively insensitive to factors such as mortality rate of engorged females. When used to simulate laboratory experiments from the literature, the model predicted most observed life-history characteristics fairly well; however, it tended to underestimate oviposition duration, incubation duration, and egg mortality and overestimate larval longevity, especially at low temperatures and high humidities. Use of the model to predict Boophilus population dynamics in hypothetical south Texas pastures showed that it reasonably generated qualitative patterns of stage-wise abundances but tended to overestimate on-host tick burdens. Collection and incorporation of data that appear not to exist for Boophilus ticks, such as larval lipid content and lipid-use rates, may improve model accuracy. Though this model needs refinements such as a smaller spatial resolution, it provides insight into responses of B. microplus or B. annulatus populations to specific weather patterns, habitat heterogeneity, and host movement.     

Modeling Diapause Termination of Rhipicephalus Appendiculatus using Statistical Tools to Detect Sudden Behavioral Changes and Time Dependencies

This paper presents statistical methodology to analyze longitudinal binary responses for which a sudden change in the response occurs in time. Probability plots, transition matrices, and change-point models and more advanced techniques such as generalized auto-regression models and hidden Markov chains are presented and applied on a study on the activity of Rhipicephalus appendiculatus, the major vector of Theileria parva, a fatal disease in cattle. This study presents individual measurements on female R. appendiculatus, which are terminating their diapause (resting status) and become active. Comprehending activity patterns is very important to better understand the ecology of R. appendiculatus. The model indicates that activity and non-activity act in an absorbing way meaning that once a tick becomes active it shows a tendency to remain active. The change-point model estimates that the sudden change in activity happens on December 10. The reaction of ticks on acceleration and changes in rainfall and temperature indicates that ticks can sense climatic changes. The study revealed the underlying not visually observable states during diapause development of the adult tick of R. appendiculatus. These states could be related to phases during the dynamic event of diapause development and post-diapause activity in R. appendiculatus.     

Multiple causes of variable tick burdens on small-mammal hosts

Blood meals by blacklegged ticks (Ixodes scapularis) on vertebrate hosts serve to transmit the agents of several zoonotic diseases, including Lyme disease, human babesiosis, and human granulocytic anaplasmosis, between host and tick. If ticks are aggregated on hosts, a small proportion of hosts may be responsible for most transmission events. Therefore, a key element in understanding and controlling the transmission of these pathogens is identifying the group(s) or individuals feeding a disproportionate number of ticks. Previous studies of tick burdens, however, have focused on differences in mean annual burdens between one or a few groups of hosts, ignoring both the strong seasonal dynamics of I. scapularis and their aggregation on hosts. We present a statistical modeling framework that predicts burdens on individual hosts throughout the year as a function of temporal-, site-, and individual-specific attributes, as well as the degree of aggregation in a negative binomial distribution. We then fit alternate versions of this model to an 11-year data set of I. scapularis burdens on white-footed mice (Peromyscus leucopus) and eastern chipmunks (Tamias striatus) to explore which factors are important to predicting tick burdens. We found that tick burdens are a complex function of many extrinsic and intrinsic factors, including seasonality. Specifically: (1) burdens on mice and chipmunks increased with densities of host-seeking ticks in a manner that suggests hosts become saturated. (2) Chipmunks draw larval ticks away from mice, which are efficient reservoirs of the Lyme disease bacterium, and mice draw nymphs away from chipmunks, which are key nymphal hosts. (3) While individual correlates were statistically important, the relationships were complex, and no group or correlate (sex, age, mass) could explain which hosts fed a disproportionate number of ticks. (4) Ticks were strongly aggregated on hosts within and across groups suggesting that some undiscovered quality of individual hosts was responsible for the aggregation. (5) Those individuals that fed more nymphs than expected, and are thus more likely to be infected with the Lyme disease agent, also tend to feed and infect more larvae than expected. Predicting which individuals those are is not yet possible.     

Localized deer absence leads to tick amplification

Deer support high tick intensities, perpetuating tick populations, but they do not support tick-borne pathogen transmission, so are dilution hosts. We test the hypothesis that absence of deer (loss of a dilution host) will result in either an increase or a reduction in tick density, and that the outcome is scale dependent. We use a complementary methodological approach starting with meta-analysis, followed up by a field experiment. Meta-analysis indicated that larger deer exclosures reduce questing (host-seeking) tick density, but as the exclosure becomes smaller (<2.5 ha) the questing tick density is increased (amplified). To determine the consequences for tick-borne pathogen transmission we carried out a field experiment, comparing the intensity of ticks that fed on hosts competent for tickborne pathogen transmission (rodents) in two small (<1 ha) deer exclosures and their replicated controls. Intensity of larval ticks on rodents was not significantly different between treatments, but nymph intensity, the tick stage responsible for tick-borne encephalitis (TBE) transmission, was higher in deer exclosures. TBE seropositive rodents were found in a deer exclosure but not in the controls. We propose that localized absence of deer (loss of a dilution host) increases tick feeding on rodents, leading to the potential for tick-borne disease hotspots.     

Mass effects mediate coexistence in competing shrews

Recent developments in metacommunity theory have raised awareness that processes occurring at regional scales might interfere with local dynamics and affect conditions for the local coexistence of competing species. Four main paradigms are recognized in this context (namely, neutral, patch-dynamics, species-sorting, and mass-effect), which differ according to the role assigned to ecological or life-history differences among competing species, as well as to the relative time scale of regional vs. local dynamics. We investigated the patterns of regional and local coexistence of two species of shrews (Crocidura russula and Sorex coronatus) sharing a similar diet (generalist insectivores) over four generations, in a spatially structured habitat at the altitudinal limit of their distributions. Local populations were small, and regional dynamics were strong, with high rates of extinction and recolonization. Niche analysis revealed significant habitat differentiation on a few important variables, including temperature and availability of winter resting sites. In sites suitable for both species, we found instances of local coexistence with no evidence of competitive exclusion. Patterns of temporal succession did not differ from random, with no suggestion of a colonization-competition trade-off. Altogether, our data provide support for the mass-effect paradigm, where regional coexistence is mediated by specialization on different habitat types, and local coexistence by rescue effects from source sites. The strong regional dynamics and demographic stochasticity, together with high dispersal rates, presumably contributed to mass effects by overriding local differences in specific competitive abilities.     

Attractive and repellent host odours guide ticks to their respective feeding sites

Summary. We have studied on-host behaviour of adults of the brown ear tick (Rhipicephalus appendiculatus Neumann, 1901) and the red-legged tick (R. evertsi Neumann, 1897), which prefer to feed mainly inside the ears and the anal regions of bovids respectively. Both species were found to be relatively successful in orienting toward and locating their respective feeding sites from different parts of the host body. Our observations suggested the operation of both avoidance (closer to the feeding site of the other) and attraction (closer to its own feeding site) responses of the ticks. In the laboratory, odour trapped from cattle ears attracted R. appendiculatus but repelled R. evertsi, whereas that from the anal region had an opposite effect. This odour-based push-pull pair of stimuli may largely account for efficient orientation behaviour of the two tick species to their respective feeding sites. We propose that such concurrent deployment of repulsive and attractive cues may be quite widespread among arthropods and related organisms that specialise on specific hosts or microenvironments in the performance of their biological functions.     

Interannual dynamics of antibody levels in naturally infected long-lived colonial birds

Little is known about the long-term persistence of specific antibodies (Ab) in natural host-parasite systems despite its potential epidemiological and ecological importance. In long-lived species, knowledge of the dynamics of individual immunological profiles can be important not only for interpreting serology results, but also for assessing transmission dynamics and the potential selective pressures acting on parasites. The aim of this paper was to investigate temporal variation in levels of specific Ab against the bacterium Borrelia burgdorferi sensu lato in adults of a long-lived colonial seabird, the Black-legged Kittiwake Rissa tridactyla. In wild populations, adults are naturally exposed each breeding season to a Borrelia vector, the tick Ixodes uriae. Breeding birds were captured during four consecutive breeding seasons, and parasite infestation quantified. Using enzyme-linked immunosorbent assay (ELISA) and immunoblots, we found that the immunological profiles of anti-Borrelia Ab were highly repeatable among years, reflecting the interannual persistence of Ab levels. We nevertheless also observed that year-to-year changes of Ab levels were related to exposure to ticks in the previous year. The long-term persistence of Ab levels may be an important mechanism of individual protection against future exposure to the microparasite. It will also affect the availability of susceptible hosts, and thus the transmission dynamics of the bacterium. These results illustrate the need to consider the dynamics of the immune response in order to better understand the evolutionary ecology of host-parasite interactions in natural populations.     

Strong self-limitation promotes the persistence of rare species

Theory has recognized a combination of niche and neutral processes each contributing, with varying importance, to species coexistence. However, long-term persistence of rare species has been difficult to produce in trait-based models of coexistence that incorporate stochastic dynamics, raising questions about how rare species persist despite such variability. Following recent evidence that rare species may experience significantly different population dynamics than dominant species, we use a plant community model to simulate the effect of disproportionately strong negative frequency dependence on the long-term persistence of the rare species in a simulated community. This strong self-limitation produces long persistence times for the rare competitors, which otherwise succumb quickly to stochastic extinction. The results suggest that the mechanism causing species to be rare in this case is the same mechanism allowing those species to persist.     

Lyme Disease and Conservation

Lyme disease is a tick-borne illness that is widespread in North America, especially in the northeastern and northcentral United States. This disease could negatively influence efforts to conserve natural populations in two ways: (1) the disease could directly affect wild animal health; and (2) tick control efforts could adversely affect natural populations and communities. Lyme disease affects several domestic animals, but symptoms have been reported in only a few wild species. Direct effects of Lyme disease on wild animal populations have not been reported, but the disease should be considered as a possible cause in cases of unexplained population declines in endemic areas. Methods available to manage ticks and Lyme disease include human self-protection techniques, manipulation of habitats and host species populations, biological control, and pesticide applications. The diversity of available techniques allows selection of approaches to minimize environmental effects by (1) emphasizing personal protection techniques, (2) carefully targeting management efforts to maximize efficiency, and (3) integrating environmentally benign techniques to improve management while avoiding broad-scale environmentally destructive approaches. The environmental effects of Lyme disease depend, to a large extent, on the methods chosen to minimize human exposure to infected ticks. Conservation biologists can help design tick management programs that effectively lower the incidence of human Lyme disease while simultaneously minimizing negative effects on natural populations.     

Modelling the dynamics of coral reef macroalgae using a Bayesian belief network approach

Macroalgae are a major benthic component of coral reefs and their dynamics influence the resilience of coral reefs to disturbance. However, the relative importance of physical and ecological processes in driving macroalgal dynamics is poorly understood. Here we develop a Bayesian belief network (BBN) model to integrate many of these processes and predict the growth of coral reef macroalgae. Bayesian belief networks use probabilistic relationships rather than deterministic rules to quantify the cause and effect assumptions. The model was developed using both new empirical data and quantified relationships elicited from previous studies. We demonstrate the efficacy of the BBN to predict the dynamics of a common Caribbean macroalgal genus Dictyota. Predictions of the model have an average accuracy of 55% (implying that 55% of the predicted categories of Dictyota cover were assigned to the correct class). Sensitivity analysis suggested that macroalgal dynamics were primarily driven by top–down processes of grazing rather than bottom–up nutrification. BBNs provide a useful framework for modelling complex systems, identifying gaps in our scientific understanding and communicating the complexities of the associated uncertainties in an explicit manner to stakeholders. We anticipate that accuracies will improve as new data are added to the model.     

Competition, predation and coexistence in a three trophic system

Simple ecological models that mostly operate with population densities using continuous variables, explain quite well the behavior of real populations. In this work we propose and discuss the continuous dynamics of a system of three species, which belongs to the well-known family of Lotka–Volterra models. In particular, the proposed model includes direct effects such as predation and competition among species, and indirect effects such as refuge. The model is proposed to explain recent studies about a group of crustacean (amphipods of genus Hyallela) found in all the plain streams and shallow lakes of the American continent. The studied system includes three compartments: algae, a strictly herbivore amphipod and an omnivore (herbivore and carnivore) one. The analysis of the model shows that there are stable extinction equilibria throughout all the parameters’ space. There are also equilibria with stable coexistence of the three species and two interesting binary equilibria: one with stable coexistence of algae and herbivore and other with coexistence between algae and omnivore amphipods. The presence of Allee effect in the algae growth and the existence of refuge for the herbivore amphipod (prey) determine a bottom-up control.     

The Threat of Disease Increases as Species Move Toward Extinction

At local scales, infectious disease is a common driver of population declines, but globally it is an infrequent contributor to species extinction and endangerment. For species at risk of extinction from disease important questions remain unanswered, including when does disease become a threat to species and does it co‐occur, predictably, with other threats? Using newly compiled data from the International Union for Conservation of Nature (IUCN) Red List, we examined the relative role and co‐occurrence of threats associated with amphibians, birds, and mammals at 6 levels of extinction risk (i.e., Red List status categories: least concern, near threatened, vulnerable, endangered, critically endangered, and extinct in the wild/extinct). We tested the null hypothesis that the proportion of species threatened by disease is the same in all 6 Red List status categories. Our approach revealed a new method for determining when disease most frequently threatens species at risk of extinction. The proportion of species threatened by disease varied significantly between IUCN status categories and linearly increased for amphibians, birds, and all species combined as these taxa move from move from least concern to critically endangered. Disease was infrequently the single contributing threat. However, when a species was negatively affected by a major threat other than disease (e.g., invasive species, land‐use change) that species was more likely to be simultaneously threatened by disease than species that had no other threats. Potential drivers of these trends include ecological factors, clustering of phylogenetically related species in Red List status categories, discovery bias among species at greater risk of extinction, and availability of data. We echo earlier calls for baseline data on the presence of parasites and pathogens in species when they show the first signs of extinction risk and arguably before. La Amenaza de Enfermedades Incrementa a Medida que las Especies se Aproximan a la Extinción     

The landscape epidemiology of foot-and-mouth disease in South Africa: A spatially explicit multi-agent simulation

This study aimed at understanding how landscape heterogeneity influences outbreaks of contagious diseases in southern Africa. Landscape attributes influence patterns of movement and behaviour of animal hosts, virus spread and survival, as well as land use practices. A multi-agent simulation was developed to represent the spatial and temporal dynamics of pathogens between human-livestock and wildlife interfaces at the fringe of large wildlife conservation areas. The model represents the three main elements associated with epidemics - populations, space, and time - to simulate direct contacts between wildlife and livestock. The dynamics of these populations emerge from interactions between agents and the landscape. The model was calibrated to represent the transmission of foot-and-mouth disease through direct contact at the border of the Kruger National Park in South Africa. In the region, African buffaloes (Syncerus caffer) act as reservoirs of the virus and spread the infection to domestic cattle bordering the park. We tested the sensitivity of various factors influencing contact rate between buffaloes and cattle, and thus the risk of foot-and-mouth disease transmission. Results show that cattle-buffalo contacts mostly depend on the range of displacements of cattle and buffaloes, as influenced by the landscape configuration, and on the number of fence breakages multiplied by the time between breakage and repair. Contacts take place not only close to water-points but also in grazing areas, within an area up to 6 km from the fence.     

The effect of deer management on the abundance of Ixodes ricinus in Scotland

The management of wildlife hosts for controlling parasites and disease has a history of mixed success. Deer can be important hosts for ticks, such as Ixodes ricinus, which is the primary vector of disease-causing zoonotic pathogens in Europe. Deer are generally managed by culling and fencing for forestry protection, habitat conservation, and commercial hunting, and in this study we test whether these deer management methods can be useful for controlling ticks, with implications for tick-borne pathogens. At different spatial scales and habitats we tested the hypotheses that tick abundance is reduced by (1) culling deer and (2) deer exclusion using fencing. We compared abundance indices of hosts and questing I. ricinus nymphs using a combination of small-scale fencing experiments on moorland, a large-scale natural experiment of fenced and unfenced pairs of forests, and cross-sectional surveys of forest and moorland areas with varying deer densities. As predicted, areas with fewer deer had fewer ticks, and fenced exclosures had dramatically fewer ticks in both large-scale forest and small-scale moorland plots. Fencing and reducing deer density were also associated with higher ground vegetation. The implications of these results on other hosts, pathogen prevalence, and disease risk are discussed. This study provides evidence of how traditional management methods of a keystone species can reduce a generalist parasite, with implications for disease risk mitigation.     

Deterministic approach to the study of the interaction predator-prey in a chemostat with predator mutual interference. Implications for the paradox of enrichment

Our understanding of predator-prey systems has progressed in recent decades mainly due to the ability to test models in chemostats. This study aimed to develop a deterministic model using differential equations to reproduce the dynamics of the interaction of a predator and a prey in a two stage chemostat focusing in the proposed previous prey dependent model of Fussmann et al. (2000) [Fussmann, G.F., Ellner, S.P., Shertzer, K.W., Hairston Jr., N.G., 2000. Crossing the Hopf bifurcation in a live predator-prey system. Science 290, 1358-1360]. The main problem with that model, but parameterized with the values obtained in this study (particularly the concentration of nutrient), was that the temporal trajectory of both the prey and the predator showed very high peaks that eventually led to the extinction of predator in all cases. In the same way the experimental time series obtained in this study does not exhibit the behavior predicted by the model of Fussman et al. On the contrary, as prey density increases, the system actually becomes more stable. Finally, the model that best explained the behavior of the predator and prey in the chemostat, at medium to high dilution rates, was the ratio dependent (algae-nitrogen) model with mutual interference measured in the chemostat (rotifer-alga) and that incorporated the age structure of the predator. Qualitative analysis of the dynamic behavior enabled evaluation of coexistence at equilibrium, coexistence on limit cycles, extinction of the predator or extinction of both populations.     

A Retrospective Evaluation of the Global Decline of Carnivores and Ungulates

Assessing temporal changes in species extinction risk is necessary for measuring conservation success or failure and for directing conservation resources toward species or regions that would benefit most. Yet, there is no long‐term picture of genuine change that allows one to associate species extinction risk trends with drivers of change or conservation actions. Through a review of 40 years of IUCN‐related literature sources on species conservation status (e.g., action plans, red‐data books), we assigned retrospective red‐list categories to the world's carnivores and ungulates (2 groups with relatively long generation times) to examine how their extinction risk has changed since the 1970s. We then aggregated species’ categories to calculate a global trend in their extinction risk over time. A decline in the conservation status of carnivores and ungulates was underway 40 years ago and has since accelerated. One quarter of all species (n = 498) moved one or more categories closer to extinction globally, while almost half of the species moved closer to extinction in Southeast Asia. The conservation status of some species improved (toward less threatened categories), but for each species that improved in status 8 deteriorated. The status of large‐bodied species, particularly those above 100 kg (including many iconic taxa), deteriorated significantly more than small‐bodied species (below 10 kg). The trends we found are likely related to geopolitical events (such as the collapse of Soviet Union), international regulations (such as CITES), shifting cultural values, and natural resource exploitation (e.g., in Southeast Asia). Retrospective assessments of global species extinction risk reduce the risk of a shifting baseline syndrome, which can affect decisions on the desirable conservation status of species. Such assessments can help conservationists identify which conservation policies and strategies are or are not helping safeguard biodiversity and thus can improve future strategies. Una Evaluación Retrospectiva de la Declinación Global de Carnívoros y Ungulados     

The Reliability of Using Population Viability Analysis for Risk Classification of Species

I examine whether or not it is appropriate to use extinction probabilities generated by population viability analyses, based on best estimates for model parameters, as criteria for listing species in Red Data Book categories as recently proposed by the World Conservation Union. Such extinction probabilities are influenced by how accurately model parameters are estimated and by how accurately the models depict actual population dynamics. I evaluate the effect of uncertainty in parameter estimation through simulations. Simulations based on Steller sea lions were used to evaluate bias and precision in estimates of probability of extinction and to consider the performance of two proposed classification schemes. Extinction time estimates were biased (because of violation of the assumption of stable age distribution) and underestimated the variability of probability of extinction for a given time (primarily because of uncertainty in parameter estimation). Bias and precision in extinction probabilities are important when these probabilities are used to compare the risk of extinction between species. Suggestions are given for population viability analysis techniques that incorporate parameter uncertainty. I conclude that testing classification schemes with simulations using quantitative performance objectives should precede adoption of quantitative listing criteria.     

Fitting probability models to population dynamics data

Methods for modeling population dynamics in probability using the generalized point process approach are developed. The life history of these populations is such that seasonal reproduction occurs during a short time. Several models are developed and analyzed. Data about two species: colonial spiders (Stegodyphus dumicola) and a migratory bird (wood thrush, Hylocichla mustelina) are used to estimate model parameters with appropriate log maximum likelihood functions. For the spiders, the model is fitted to provide evolutionary feasible colony size based on maximum likelihood estimates of fecundity and survival data. For the migratory bird species, a maximum likelihood estimates are derived for the fecundity and survival rates of young and adult birds and immigration rate. The presented approach allows computation of quantities of interest such as probability of extinction and average time to extinction.     

Extinction Debts and Risks Faced by Abundant Species

A recent model indicating that good competitiors and abundant species face the greatest risk of extinction from habitat destruction is critically examined. The conclusions drawn from the model are shown to rely on a number of assumptions regarding the mechanism of species coexistence, the relationship between abundance and competitive ability, and spatial characteristics of habitat destruction. The generality of these assumptions is questioned. Of particular concern are the assumptions that good competitors are poor dispersers, and that good competitors are the most abundant species. Furthermore, we suggest that the spatial scale of metapopulation dynamics in the model may not be appropriate for representing impacts of habitat destrustion. Empirical evidence is discussed indicating the limited applicability of the model for describing effects of habitat destruction on risks of species extinctions. Examples from a number of fragmented systems demonstrate that poor competitors and rare species are vulnerable to habitat destruction.