Improving Aquatic Warbler Population Assessments by Accounting for Imperfect Detection

Monitoring programs designed to assess changes in population size over time need to account for imperfect detection and provide estimates of precision around annual abundance estimates. Especially for species dependent on conservation management, robust monitoring is essential to evaluate the effectiveness of management. Many bird species of temperate grasslands depend on specific conservation management to maintain suitable breeding habitat. One such species is the Aquatic Warbler (Acrocephalus paludicola), which breeds in open fen mires in Central Europe. Aquatic Warbler populations have so far been assessed using a complete survey that aims to enumerate all singing males over a large area. Because this approach provides no estimate of precision and does not account for observation error, detecting moderate population changes is challenging. From 2011 to 2013 we trialled a new line transect sampling monitoring design in the Biebrza valley, Poland, to estimate abundance of singing male Aquatic Warblers. We surveyed Aquatic Warblers repeatedly along 50 randomly placed 1-km transects, and used binomial mixture models to estimate abundances per transect. The repeated line transect sampling required 150 observer days, and thus less effort than the traditional ‘full count’ approach (175 observer days). Aquatic Warbler abundance was highest at intermediate water levels, and detection probability varied between years and was influenced by vegetation height. A power analysis indicated that our line transect sampling design had a power of 68% to detect a 20% population change over 10 years, whereas raw count data had a 9% power to detect the same trend. Thus, by accounting for imperfect detection we increased the power to detect population changes. We recommend to adopt the repeated line transect sampling approach for monitoring Aquatic Warblers in Poland and in other important breeding areas to monitor changes in population size and the effects of habitat management.     

Accounting for Imperfect Detection in Ecology: A Quantitative Review

Detection in studies of species abundance and distribution is often imperfect. Assuming perfect detection introduces bias into estimation that can weaken inference upon which understanding and policy are based. Despite availability of numerous methods designed to address this assumption, many refereed papers in ecology fail to account for non-detection error. We conducted a quantitative literature review of 537 ecological articles to measure the degree to which studies of different taxa, at various scales, and over time have accounted for imperfect detection. Overall, just 23% of articles accounted for imperfect detection. The probability that an article incorporated imperfect detection increased with time and varied among taxa studied; studies of vertebrates were more likely to incorporate imperfect detection. Among articles that reported detection probability, 70% contained per-survey estimates of detection that were less than 0.5. For articles in which constancy of detection was tested, 86% reported significant variation. We hope that our findings prompt more ecologists to consider carefully the detection process when designing studies and analyzing results, especially for sub-disciplines where incorporation of imperfect detection in study design and analysis so far has been lacking.     

Occupancy Modeling for Improved Accuracy and Understanding of Pathogen Prevalence and Dynamics

Most pathogen detection tests are imperfect, with a sensitivity < 100%, thereby resulting in the potential for a false negative, where a pathogen is present but not detected. False negatives in a sample inflate the number of non-detections, negatively biasing estimates of pathogen prevalence. Histological examination of tissues as a diagnostic test can be advantageous as multiple pathogens can be examined and providing important information on associated pathological changes to the host. However, it is usually less sensitive than molecular or microbiological tests for specific pathogens. Our study objectives were to 1) develop a hierarchical occupancy model to examine pathogen prevalence in spring Chinook salmon Oncorhynchus tshawytscha and their distribution among host tissues 2) use the model to estimate pathogen-specific test sensitivities and infection rates, and 3) illustrate the effect of using replicate within host sampling on sample sizes required to detect a pathogen. We examined histological sections of replicate tissue samples from spring Chinook salmon O. tshawytscha collected after spawning for common pathogens seen in this population: Apophallus/echinostome metacercariae, Parvicapsula minibicornis, Nanophyetus salmincola/ metacercariae, and Renibacterium salmoninarum. A hierarchical occupancy model was developed to estimate pathogen and tissue-specific test sensitivities and unbiased estimation of host- and organ-level infection rates. Model estimated sensitivities and host- and organ-level infections rates varied among pathogens and model estimated infection rate was higher than prevalence unadjusted for test sensitivity, confirming that prevalence unadjusted for test sensitivity was negatively biased. The modeling approach provided an analytical approach for using hierarchically structured pathogen detection data from lower sensitivity diagnostic tests, such as histology, to obtain unbiased pathogen prevalence estimates with associated uncertainties. Accounting for test sensitivity using within host replicate samples also required fewer individual fish to be sampled. This approach is useful for evaluating pathogen or microbe community dynamics when test sensitivity is <100%.     

Accounting for Imperfect Detection Is Critical for Inferring Marine Turtle Nesting Population Trends

Assessments of population trends based on time-series counts of individuals are complicated by imperfect detection, which can lead to serious misinterpretations of data. Population trends of threatened marine turtles worldwide are usually based on counts of nests or nesting females. We analyze 39 years of nest-count, female-count, and capture-mark-recapture (CMR) data for nesting loggerhead turtles (Caretta caretta) on Wassaw Island, Georgia, USA. Annual counts of nests and females, not corrected for imperfect detection, yield significant, positive trends in abundance. However, multistate open robust design modeling of CMR data that accounts for changes in imperfect detection reveals that the annual abundance of nesting females has remained essentially constant over the 39-year period. The dichotomy could result from improvements in surveys or increased within-season nest-site fidelity in females, either of which would increase detection probability. For the first time in a marine turtle population, we compare results of population trend analyses that do and do not account for imperfect detection and demonstrate the potential for erroneous conclusions. Past assessments of marine turtle population trends based exclusively on count data should be interpreted with caution and re-evaluated when possible. These concerns apply equally to population assessments of all species with imperfect detection.     

Occupancy Models for Monitoring Marine Fish: A Bayesian Hierarchical Approach to Model Imperfect Detection with a Novel Gear Combination

Occupancy models using incidence data collected repeatedly at sites across the range of a population are increasingly employed to infer patterns and processes influencing population distribution and dynamics. While such work is common in terrestrial systems, fewer examples exist in marine applications. This disparity likely exists because the replicate samples required by these models to account for imperfect detection are often impractical to obtain when surveying aquatic organisms, particularly fishes. We employ simultaneous sampling using fish traps and novel underwater camera observations to generate the requisite replicate samples for occupancy models of red snapper, a reef fish species. Since the replicate samples are collected simultaneously by multiple sampling devices, many typical problems encountered when obtaining replicate observations are avoided. Our results suggest that augmenting traditional fish trap sampling with camera observations not only doubled the probability of detecting red snapper in reef habitats off the Southeast coast of the United States, but supplied the necessary observations to infer factors influencing population distribution and abundance while accounting for imperfect detection. We found that detection probabilities tended to be higher for camera traps than traditional fish traps. Furthermore, camera trap detections were influenced by the current direction and turbidity of the water, indicating that collecting data on these variables is important for future monitoring. These models indicate that the distribution and abundance of this species is more heavily influenced by latitude and depth than by micro-scale reef characteristics lending credence to previous characterizations of red snapper as a reef habitat generalist. This study demonstrates the utility of simultaneous sampling devices, including camera traps, in aquatic environments to inform occupancy models and account for imperfect detection when describing factors influencing fish population distribution and dynamics.     

Impact of Mistletoe Triterpene Acids on the Uptake of Mistletoe Lectin by Cultured Tumor Cells

Complementary treatment possibilities for the therapy of cancer are increasing in demand due to the severe side effects of the standard cytostatics used in the first-line therapy. A common approach as a complementary treatment is the use of aqueous extracts of Viscum album L. (Santalaceace). The therapeutic activity of these extracts is attributed to Mistletoe lectins which are Ribosome-inactivating proteins type II. Besides these main constituents the extract of Viscum album L. comprises also a mixture of lipophilic ingredients like triterpene acids of the oleanane, lupane and ursane type. However, these constituents are not contained in commercially available aqueous extracts due to their high lipophilicity and insolubility in aqueous extraction media. To understand the impact of the extract ingredients in cancer therapy, the intracellular uptake of the mistletoe lectin I (ML) by cultured tumor cells was investigated in relation to the mistletoe triterpene acids, mainly oleanolic acid. Firstly, these hydrophobic triterpene acids were solubilized using cyclodextrins (“TT” extract). Afterwards, the uptake of either single compounds (isolated ML and the aqueous “viscum” extract) or in combination with the TT extract (ML+TT, viscumTT), was analyzed. The uptake of ML was studied inTHP-1-, HL-60-, 143B- and Ewing TC-71-cells and determined after 30, 60 and 120 minutes by an enzyme linked immunosorbent assay which quantifies the A-chain of the hololectin. It could be shown that the intracellular uptake after 120 minutes amounted to 20% in all cell lines after incubation with viscumTT. The studies further revealed that the uptake in THP-1-, HL-60- and Ewing TC-71-cells was independent of the addition of TT extract. Interestingly, the uptake of ML by 143B-cells could only be measured after addition of triterpenes pointing to resistance to mistletoe lectin.     

Quantification and Modeling of Plasmid Mobilization on Seeds and Roots

Mobilization frequencies of the nonconjugative plasmid pMON5003 were quantified using Escherichia coli TB1(pRK2013) as donor of a helper plasmid, E. coli M182 (pMON5003) as donor of the nonconjugative plasmid, and Pseudomonas fluorescens as recipient. Initial mating experiments were conducted in nutrient and minimal salts media and pea seed exudates. Mobilization rates were higher during early stationary growth of donors, helpers, and recipients. Numbers of transconjugants were higher in biparental matings when donors contained both conjugative and nonconjugative plasmids, versus tri-parental matings. A mathematical model was developed to predict a nonconjugative plasmid transfer rate parameter (δ), estimating the proportion of conjugative matings in which a plasmid is mobilized. Values of δ ranged from 8 × 10⁻³ to 7.9 × 10⁻¹. Transfer frequencies for pMON5003 from E. coli to P. fluorescens on pea seeds and roots were determined. Transconjugants (P. fluorescens 2-79 (pMON5003)) were isolated from seeds, roots, and soil, but mobilization frequencies were lower than in liquid media.     

Occupancy Modeling Reveals Interspecific Variation in Habitat Use and Negative Effects of Dogs on Lemur Populations

International Journal of Primatology - Effective, targeted management and conservation plans for wildlife populations require reliable population sampling and estimation. Unfortunately, robust,...     

Modeling Disease Vector Occurrence when Detection Is Imperfect: Infestation of Amazonian Palm Trees by Triatomine Bugs at Three Spatial Scales

Background

Failure to detect a disease agent or vector where it actually occurs constitutes a serious drawback in epidemiology. In the pervasive situation where no sampling technique is perfect, the explicit analytical treatment of detection failure becomes a key step in the estimation of epidemiological parameters. We illustrate this approach with a study of Attalea palm tree infestation by Rhodnius spp. (Triatominae), the most important vectors of Chagas disease (CD) in northern South America.

Methodology/Principal Findings

The probability of detecting triatomines in infested palms is estimated by repeatedly sampling each palm. This knowledge is used to derive an unbiased estimate of the biologically relevant probability of palm infestation. We combine maximum-likelihood analysis and information-theoretic model selection to test the relationships between environmental covariates and infestation of 298 Amazonian palm trees over three spatial scales: region within Amazonia, landscape, and individual palm. Palm infestation estimates are high (40–60%) across regions, and well above the observed infestation rate (24%). Detection probability is higher (∼0.55 on average) in the richest-soil region than elsewhere (∼0.08). Infestation estimates are similar in forest and rural areas, but lower in urban landscapes. Finally, individual palm covariates (accumulated organic matter and stem height) explain most of infestation rate variation.

Conclusions/Significance

Individual palm attributes appear as key drivers of infestation, suggesting that CD surveillance must incorporate local-scale knowledge and that peridomestic palm tree management might help lower transmission risk. Vector populations are probably denser in rich-soil sub-regions, where CD prevalence tends to be higher; this suggests a target for research on broad-scale risk mapping. Landscape-scale effects indicate that palm triatomine populations can endure deforestation in rural areas, but become rarer in heavily disturbed urban settings. Our methodological approach has wide application in infectious disease research; by improving eco-epidemiological parameter estimation, it can also significantly strengthen vector surveillance-control strategies.     

Modeling Disease Vector Occurrence When Detection Is Imperfect II: Drivers of Site-Occupancy by Synanthropic Triatoma brasiliensis in the Brazilian Northeast

Background

Understanding the drivers of habitat selection by insect disease vectors is instrumental to the design and operation of rational control-surveillance systems. One pervasive yet often overlooked drawback of vector studies is that detection failures result in some sites being misclassified as uninfested; naïve infestation indices are therefore biased, and this can confound our view of vector habitat preferences. Here, we present an initial attempt at applying methods that explicitly account for imperfect detection to investigate the ecology of Chagas disease vectors in man-made environments.

Methodology

We combined triplicate-sampling of individual ecotopes (n = 203) and site-occupancy models (SOMs) to test a suite of pre-specified hypotheses about habitat selection by Triatoma brasiliensis. SOM results were compared with those of standard generalized linear models (GLMs) that assume perfect detection even with single bug-searches.

Principal Findings

Triatoma brasiliensis was strongly associated with key hosts (native rodents, goats/sheep and, to a lesser extent, fowl) in peridomestic environments; ecotope structure had, in comparison, small to negligible effects, although wooden ecotopes were slightly preferred. We found evidence of dwelling-level aggregation of infestation foci; when there was one such focus, same-dwelling ecotopes, whether houses or peridomestic structures, were more likely to become infested too. GLMs yielded negatively-biased covariate effect estimates and standard errors; both were, on average, about four times smaller than those derived from SOMs.

Conclusions/Significance

Our results confirm substantial population-level ecological heterogeneity in T. brasiliensis. They also suggest that, at least in some sites, control of this species may benefit from peridomestic rodent control and changes in goat/sheep husbandry practices. Finally, our comparative analyses highlight the importance of accounting for the various sources of uncertainty inherent to vector studies, including imperfect detection. We anticipate that future research on infectious disease ecology will increasingly rely on approaches akin to those described here.     

Carbohydrate-mediated Recognition of Larval Mosquito Hosts by Romanomermis culicivorax

Proteases, glycosidases, and lectins were tested and the results supported a role in host recognition for glycoproteins containing β-glucose and α-mannose on the cuticular surface of host and parasite. Carbohydrates containing α-glucose, galactose, fucose, or N-acetylglucosamine residues apparently are not involved in nematode attachment. Chitin or a related N-acetylglucosamine polymer was found in R. culicivorax preparasites. Treatment of preparasites with neuraminidase, which hydrolyzes sialic acids, increased nematode attachment to Anopheles freeborni larvae.     

Modeling Dengue Vector Dynamics under Imperfect Detection: Three Years of Site-Occupancy by Aedes aegypti and Aedes albopictus in Urban Amazonia

Aedes aegypti and Ae. albopictus are the vectors of dengue, the most important arboviral disease of humans. To date, Aedes ecology studies have assumed that the vectors are truly absent from sites where they are not detected; since no perfect detection method exists, this assumption is questionable. Imperfect detection may bias estimates of key vector surveillance/control parameters, including site-occupancy (infestation) rates and control intervention effects. We used a modeling approach that explicitly accounts for imperfect detection and a 38-month, 55-site detection/non-detection dataset to quantify the effects of municipality/state control interventions on Aedes site-occupancy dynamics, considering meteorological and dwelling-level covariates. Ae. aegypti site-occupancy estimates (mean 0.91; range 0.79–0.97) were much higher than reported by routine surveillance based on ‘rapid larval surveys’ (0.03; 0.02–0.11) and moderately higher than directly ascertained with oviposition traps (0.68; 0.50–0.91). Regular control campaigns based on breeding-site elimination had no measurable effects on the probabilities of dwelling infestation by dengue vectors. Site-occupancy fluctuated seasonally, mainly due to the negative effects of high maximum (Ae. aegypti) and minimum (Ae. albopictus) summer temperatures (June-September). Rainfall and dwelling-level covariates were poor predictors of occupancy. The marked contrast between our estimates of adult vector presence and the results from ‘rapid larval surveys’ suggests, together with the lack of effect of local control campaigns on infestation, that many Aedes breeding sites were overlooked by vector control agents in our study setting. Better sampling strategies are urgently needed, particularly for the reliable assessment of infestation rates in the context of control program management. The approach we present here, combining oviposition traps and site-occupancy models, could greatly contribute to that crucial aim.     

Conservation Assessments of Arboreal Mammals in Difficult Terrain: Occupancy Modeling of Pileated Gibbons (Hylobates pileatus)

Long-term monitoring programs, wildlife surveys, and other research involving species population assessment require reliable data on population status. Given the logistically challenging nature of some species’ habitats and cryptic behaviors, collecting these data can prove to be a considerable barrier. We used detection/nondetection data from pileated gibbons (Hylobates pileatus) in the Cardamom Mountains of southwest Cambodia to estimate their population occupancy and detectability. We modeled occupancy using elevation, tree height, tree density, tree diversity, and disturbance covariates. Modeling demonstrated that 83% of the sites are occupied by Hylobates pileatus and that the detectability of the species varies positively with elevation. No clear relationship between habitat quality covariates and occupancy of Hylobates pileatus emerged. Effort analysis based on model estimates demonstrated that at high elevations, less than half the number of site visits is needed to attain the same detectability estimate precision as across all elevations. We suggest that human activities at low elevations, which affect forest composition, are the central factors impacting the detectability and occupancy of Hylobates pileatus. Longer sampling durations and/or a higher number of site visits, especially at lower elevations, increase precision of the occupancy estimator for the least effort. For effective future monitoring and research for this and similar species, using this relatively simple method, applied with repeat site visits, would allow a longitudinal comparison of detection at sites in difficult terrain.     

Modeling Facilitative Sugar Transporters: Transitions Between Single and Double Ligand Occupancy of Multiconformational Channel Models Explain Anomalous Kinetics

The four-state simple carrier model (SCM) is employed to describe ligand translocation by diverse passive membrane transporters. However, its application to systems like facilitative sugar transporters (GLUTs) is controversial: unidirectional fluxes under zero-trans and equilibrium-exchange experimental conditions fit a SCM, but flux data from infinite-cis and infinite-trans experiments appear not to fit the same SCM. More complex kinetic models have been proposed to explain this ``anomalous' behavior of GLUTs, but none of them accounts for all the experimental findings. We propose an alternative model in which GLUTs are channels subject to conformational transitions, and further assume that the results from zero-trans and equilibrium-exchange experiments as well as trans-effects corresponds to a single-occupancy channel regime, whereas the results from the infinite-cis and infinite-trans experiments correspond to a regime including higher channel occupancies. We test the plausibility of this hypothesis by studying a kinetic model of a two-site channel with two conformational states. In each state, the channel can bind the ligand from only one of the compartments. Under single-occupancy, for conditions corresponding to zero-trans and equilibrium-exchange experiments, the model behaves as a SCM capable of exhibiting trans-stimulations. For a regime including higher degrees of occupancy and infinite-cis and infinite-trans conditions, the same channel model can exhibit a behavior qualitatively similar to a SCM, albeit with kinetic parameters different from those for the single-occupancy regime. Numerical results obtained with our model are consistent with available experimental data on facilitative glucose transport across erythrocyte membranes. Hence, if GLUTs are multiconformational channels, their particular kinetic properties can result from transitions between single and double channel occupancies. Received: 12 April 1995/Revised: 28 August 1995     

Invigoration of Cotton Seedlings by Treatment of Seeds for Pregermination Activities

Incubation of cotton seeds (Gossypium hirsutum, cv. Acala S.J.2) at 20 °C and 95% r.h. for up to 12 d results in an increasein seed water content and in a higher rate of seedling development.When seed vigour is measured by tolerance to high temperaturestorage (aging conditions) or tolerance to low temperature andsalinity during germination, seeds incubated for up to 4 d aremore vigorous than the control seeds. Hence, such a presowingtreatment of seed could be used for seed invigoration. As theincubation proceeds, although a higher growth rate of seedlingsis obtained at optimal conditions, the tolerance to stress conditionsdeclines proportional to the duration of incubation. Results of chemical and biochemical examinations of the incubatedseeds are compared with those of seeds during normal imbibitionfor germination. The early stage of germination (up to 4 h)is accompanied by a decrease in reducing sugars and amino acids.At the later stage, an increase of these components and a decreasein the lipid fraction occur. During the first 4 h, an increaseand decrease of phosphoenolpyruvate carboxylase and of malicdehydrogenase occur. According to the chemical and biochemicalmarkers, it is evident that seed treatment at 20 °C and95% r.h. results in pregermination biochemical activities. Thefirst 4 d seem to be equivalent to the first 3 h of germinationunder normal conditons. At this period of time, degradationprocesses are taking place. If incubation is continued the resynthesisstage appears to be retarded by the low moisture available andtherefore degradation processes continue, resulting in lossof seed vigour. The resynthesis ability may therefore be a prerequisitefor the following steps in seed germination.     

Lack of Evidence for Cospeciation Between Retroelements and Their Hosts

Some literature is available on cospeciation and on reconstructing the phylogenetic relationships of retroelements, but relatively little consideration has been given to whether there is cospeciation between retroelements and their hosts. Here we address this problem in detail. We conclude that there is no significant evidence for cospeciation between retroelements and their hosts. This conclusion was reached by noting that the branching order of the two phylogenies was no more similar than would be expected by chance. Received: 18 February 1999 / Accepted: 1 October 1999